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January 22, 2019; 92 (4) Video NeuroImages

Face-selective neurons in the vicinity of the human fusiform face area

View ORCID ProfileVadim Axelrod, Camille Rozier, Tal Seidel Malkinson, Katia Lehongre, Claude Adam, Virginie Lambrecq, Vincent Navarro, Lionel Naccache
First published January 21, 2019, DOI: https://doi.org/10.1212/WNL.0000000000006806
Vadim Axelrod
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
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
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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Katia Lehongre
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
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
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
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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Lionel Naccache
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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Face-selective neurons in the vicinity of the human fusiform face area
Vadim Axelrod, Camille Rozier, Tal Seidel Malkinson, Katia Lehongre, Claude Adam, Virginie Lambrecq, Vincent Navarro, Lionel Naccache
Neurology Jan 2019, 92 (4) 197-198; DOI: 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 area2 (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).

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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, 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 (office{at}charliechapin.com).

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.Download Supplementary Video 1 via http://dx.doi.org/10.1212/006806_Video_1

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.

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.

Disclosure

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

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.

Footnotes

  • Go to Neurology.org/N for full disclosures.

  • © 2019 American Academy of Neurology

References

  1. 1.↵
    1. Bentin S,
    2. Allison T,
    3. Puce A,
    4. Perez E,
    5. McCarthy G
    . Electrophysiological studies of face perception in humans. J Cogn Neurosci 1996;8:551–565.
    OpenUrlCrossRefPubMed
  2. 2.↵
    1. Kanwisher N,
    2. 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.
    OpenUrlCrossRefPubMed

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