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January 21, 2019
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Face-selective neurons in the vicinity of the human fusiform face area

Vadim Axelrod, PhD https://orcid.org/0000-0003-2512-327X, Camille Rozier, PhD, Tal Seidel Malkinson, PhD, Katia Lehongre, PhD, Claude Adam, MD, PhD, Virginie Lambrecq, MD, PhD, Vincent Navarro, MD, PhD, and Lionel Naccache, MD, PhDAuthors Info & Affiliations
January 22, 2019 issue
92 (4) 197-198
https://doi.org/10.1212/WNL.0000000000006806
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Face perception is thought to be mediated by neural activity in the occipital and posterior temporal cortex. 1,2 However, the face-selective neurons at the cellular level in these areas in humans have never been demonstrated. We had a rare opportunity to record intracranial multi-unit activity in an epilepsy patient near the fusiform face area 2 (figure 1A). We identified 2 units with highly face-selective response to static images of familiar (famous) and unfamiliar faces (figure 1B and video 1; figure e-1a, doi.org/10.5061/dryad.81t0fq1) as well as to human and animal faces that appeared in a movie (figure 1C, video 1, figure e-1b).
Figure Recording location and the results of unit 1
1(A) Anatomic image with overlaid individual functional MRI activations (contrast: face > objects; p < 0.001, uncorrected). (B) Experiment with static images: left is a raster plot (horizontal gray lines separate the different conditions); right is across trials' mean instantaneous firing rate per condition. Note the high face-selectivity in both face conditions. Credits for images: unfamiliar scene: Avishai Taicher (CC BY 2.5), familiar scene: user: ewrfpiuqwnpiqfnpwi (CC BY 2.5), unfamiliar face: Moshe Sinai, familiar face: shutterstock.com. (C) Movie experiment (6-minute fragment of The Circus silent film). Movie frames (n = 1,800) were binned into 4 different types of frames of the movie: large, medium, small, and no faces. Note the higher average firing rate for frames with large faces. Error bars denote the standard error of mean. *Human electrophysiology does not permit us to establish unequivocally whether the units were within the boundaries of the fusiform face area (FFA; e-Methods, https://doi.org/10.5061/dryad.81t0fq1). Permission to reproduce material from The Circus movie: Charles Chaplin, The Circus; Copyright Roy Export SAS; all rights reserved ([email protected]).
Video 1
Firing rate for representative static images and the fragment of the movie. X axis is time (in seconds). Note the higher firing rate to face stimuli. Due to copyright restrictions, in this demonstration several images that had been used in the experiment have been substituted with similar equivalent images. Credit for the images is specified under each image.

Acknowledgment

The authors thank the patient for participating in this study, Leila Reddy for advice on using the wave_clus tool, and Roy Export SAS for permission to use material from The Circus.

References

1.
Bentin S, Allison T, Puce A, Perez E, McCarthy G. Electrophysiological studies of face perception in humans. J Cogn Neurosci 1996;8:551–565.
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2.
Kanwisher N, Yovel G. The fusiform face area: a cortical region specialized for the perception of faces. Philos Trans R Soc B Biol Sci 2006;361:2109–2128.
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Information & Authors

Information

Published In

Neurology®
Volume 92 • Number 4 • January 22, 2019
Pages: 197-198
PubMed: 30665911

Copyright

© 2019 American Academy of Neurology.

Publication History

Published online: January 21, 2019
Published in print: January 22, 2019

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Disclosure

The authors report no disclosures relevant to the manuscript. Go to Neurology.org/N for full disclosures.

Study Funding

This study was supported by an Alon Fellowship for outstanding young faculty members by the Israeli Council for Higher Education (V.A.), Israel Science Foundation (57/15) and Marie Skłodowska-Curie (702577) fellowships (T.S.M.), and the program “Investissements d'avenir” ANR-10-IAIHU-06 and the ICM-OCIRP.

Authors

Affiliations & Disclosures

Vadim Axelrod, PhD https://orcid.org/0000-0003-2512-327X
From The Gonda Multidisciplinary Brain Research Center (V.A.), Bar Ilan University, Ramat Gan, Israel; Institut National de la Santé et de la Recherche Médicale Unité 1127 (C.R., T.S.M., K.L., V.L., V.N., L.N.), Centre National de la Recherche Scientifique Unité Mixte de Recherche (UMR) 7225, Sorbonne Université, Université Pierre-et-Marie-Curie Univ Paris 06 UMR S 1127, Institut du Cerveau et de la Moelle Épinière; Centre de NeuroImagerie de Recherche–CENIR (K.L.), Institute of Brain and Spine, UMRS 1127, CNRS UMR 7225, Pitié‐Salpêtriere Hospital; Epilepsy Unit and Neurophysiology Department (C.A., V.L., V.N.), AP‐HP, GH Pitie‐Salpêtrière‐Charles Foix; and Departments of Neurology and Neurophysiology (L.N.), AP-HP, Groupe Hospitalier Pitié-Salpêtrière, Paris, France.
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Camille Rozier, PhD
From The Gonda Multidisciplinary Brain Research Center (V.A.), Bar Ilan University, Ramat Gan, Israel; Institut National de la Santé et de la Recherche Médicale Unité 1127 (C.R., T.S.M., K.L., V.L., V.N., L.N.), Centre National de la Recherche Scientifique Unité Mixte de Recherche (UMR) 7225, Sorbonne Université, Université Pierre-et-Marie-Curie Univ Paris 06 UMR S 1127, Institut du Cerveau et de la Moelle Épinière; Centre de NeuroImagerie de Recherche–CENIR (K.L.), Institute of Brain and Spine, UMRS 1127, CNRS UMR 7225, Pitié‐Salpêtriere Hospital; Epilepsy Unit and Neurophysiology Department (C.A., V.L., V.N.), AP‐HP, GH Pitie‐Salpêtrière‐Charles Foix; and Departments of Neurology and Neurophysiology (L.N.), AP-HP, Groupe Hospitalier Pitié-Salpêtrière, Paris, France.
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Tal Seidel Malkinson, PhD
From The Gonda Multidisciplinary Brain Research Center (V.A.), Bar Ilan University, Ramat Gan, Israel; Institut National de la Santé et de la Recherche Médicale Unité 1127 (C.R., T.S.M., K.L., V.L., V.N., L.N.), Centre National de la Recherche Scientifique Unité Mixte de Recherche (UMR) 7225, Sorbonne Université, Université Pierre-et-Marie-Curie Univ Paris 06 UMR S 1127, Institut du Cerveau et de la Moelle Épinière; Centre de NeuroImagerie de Recherche–CENIR (K.L.), Institute of Brain and Spine, UMRS 1127, CNRS UMR 7225, Pitié‐Salpêtriere Hospital; Epilepsy Unit and Neurophysiology Department (C.A., V.L., V.N.), AP‐HP, GH Pitie‐Salpêtrière‐Charles Foix; and Departments of Neurology and Neurophysiology (L.N.), AP-HP, Groupe Hospitalier Pitié-Salpêtrière, Paris, France.
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(1)Agence Nationale de la Recherche, France, ANR-16-CE37-0005 - BRANDY, co-investigator, 2017-present
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Katia Lehongre, PhD
From The Gonda Multidisciplinary Brain Research Center (V.A.), Bar Ilan University, Ramat Gan, Israel; Institut National de la Santé et de la Recherche Médicale Unité 1127 (C.R., T.S.M., K.L., V.L., V.N., L.N.), Centre National de la Recherche Scientifique Unité Mixte de Recherche (UMR) 7225, Sorbonne Université, Université Pierre-et-Marie-Curie Univ Paris 06 UMR S 1127, Institut du Cerveau et de la Moelle Épinière; Centre de NeuroImagerie de Recherche–CENIR (K.L.), Institute of Brain and Spine, UMRS 1127, CNRS UMR 7225, Pitié‐Salpêtriere Hospital; Epilepsy Unit and Neurophysiology Department (C.A., V.L., V.N.), AP‐HP, GH Pitie‐Salpêtrière‐Charles Foix; and Departments of Neurology and Neurophysiology (L.N.), AP-HP, Groupe Hospitalier Pitié-Salpêtrière, Paris, France.
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Claude Adam, MD, PhD
From The Gonda Multidisciplinary Brain Research Center (V.A.), Bar Ilan University, Ramat Gan, Israel; Institut National de la Santé et de la Recherche Médicale Unité 1127 (C.R., T.S.M., K.L., V.L., V.N., L.N.), Centre National de la Recherche Scientifique Unité Mixte de Recherche (UMR) 7225, Sorbonne Université, Université Pierre-et-Marie-Curie Univ Paris 06 UMR S 1127, Institut du Cerveau et de la Moelle Épinière; Centre de NeuroImagerie de Recherche–CENIR (K.L.), Institute of Brain and Spine, UMRS 1127, CNRS UMR 7225, Pitié‐Salpêtriere Hospital; Epilepsy Unit and Neurophysiology Department (C.A., V.L., V.N.), AP‐HP, GH Pitie‐Salpêtrière‐Charles Foix; and Departments of Neurology and Neurophysiology (L.N.), AP-HP, Groupe Hospitalier Pitié-Salpêtrière, Paris, France.
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Virginie Lambrecq, MD, PhD
From The Gonda Multidisciplinary Brain Research Center (V.A.), Bar Ilan University, Ramat Gan, Israel; Institut National de la Santé et de la Recherche Médicale Unité 1127 (C.R., T.S.M., K.L., V.L., V.N., L.N.), Centre National de la Recherche Scientifique Unité Mixte de Recherche (UMR) 7225, Sorbonne Université, Université Pierre-et-Marie-Curie Univ Paris 06 UMR S 1127, Institut du Cerveau et de la Moelle Épinière; Centre de NeuroImagerie de Recherche–CENIR (K.L.), Institute of Brain and Spine, UMRS 1127, CNRS UMR 7225, Pitié‐Salpêtriere Hospital; Epilepsy Unit and Neurophysiology Department (C.A., V.L., V.N.), AP‐HP, GH Pitie‐Salpêtrière‐Charles Foix; and Departments of Neurology and Neurophysiology (L.N.), AP-HP, Groupe Hospitalier Pitié-Salpêtrière, Paris, France.
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Vincent Navarro, MD, PhD
From The Gonda Multidisciplinary Brain Research Center (V.A.), Bar Ilan University, Ramat Gan, Israel; Institut National de la Santé et de la Recherche Médicale Unité 1127 (C.R., T.S.M., K.L., V.L., V.N., L.N.), Centre National de la Recherche Scientifique Unité Mixte de Recherche (UMR) 7225, Sorbonne Université, Université Pierre-et-Marie-Curie Univ Paris 06 UMR S 1127, Institut du Cerveau et de la Moelle Épinière; Centre de NeuroImagerie de Recherche–CENIR (K.L.), Institute of Brain and Spine, UMRS 1127, CNRS UMR 7225, Pitié‐Salpêtriere Hospital; Epilepsy Unit and Neurophysiology Department (C.A., V.L., V.N.), AP‐HP, GH Pitie‐Salpêtrière‐Charles Foix; and Departments of Neurology and Neurophysiology (L.N.), AP-HP, Groupe Hospitalier Pitié-Salpêtrière, Paris, France.
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Scientific advisory board for EISAI SAS, France, for LivaNova, France, and for Bioserenity, France
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Funding for travel and speaker honoraria from EISAI SAS, France and from UCB pharma, France
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support from the program ?Investissements d?avenir? ANR-10-IAIHU-06
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Lionel Naccache, MD, PhD
From The Gonda Multidisciplinary Brain Research Center (V.A.), Bar Ilan University, Ramat Gan, Israel; Institut National de la Santé et de la Recherche Médicale Unité 1127 (C.R., T.S.M., K.L., V.L., V.N., L.N.), Centre National de la Recherche Scientifique Unité Mixte de Recherche (UMR) 7225, Sorbonne Université, Université Pierre-et-Marie-Curie Univ Paris 06 UMR S 1127, Institut du Cerveau et de la Moelle Épinière; Centre de NeuroImagerie de Recherche–CENIR (K.L.), Institute of Brain and Spine, UMRS 1127, CNRS UMR 7225, Pitié‐Salpêtriere Hospital; Epilepsy Unit and Neurophysiology Department (C.A., V.L., V.N.), AP‐HP, GH Pitie‐Salpêtrière‐Charles Foix; and Departments of Neurology and Neurophysiology (L.N.), AP-HP, Groupe Hospitalier Pitié-Salpêtrière, Paris, France.
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I received Royalties from the Publisher of my last two essays : 'Parlez vous cerveau?' Odile Jacob Publisher, Paris, France (2018),'Le chant du signe' Odile Jacob Publisher, Paris, France (2017)
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Notes

Correspondence Dr. Axelrod [email protected]
Go to Neurology.org/N for full disclosures.

Author Contributions

V. Axelrod: conceiving the study, designing and preparing the experiments, analyzing the data, writing, editing and revising the manuscript. C. Rozier: data acquisition. T.S. Malkinson: data acquisition, editing the manuscript. K. Lehongre: responsibility for intracranial recording infrastructure, editing the manuscript. C. Adam: responsibility for intracranial recording infrastructure. V. Lambrecq: responsibility for intracranial recording infrastructure, editing the manuscript. V. Navarro: responsibility for intracranial recording infrastructure, editing the manuscript. L. Naccache: conceiving the study, supervising the project, editing the manuscript.

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