Intracerebral electrical stimulation of a face-selective area in the right inferior occipital cortex impairs individual face discrimination

During intracerebral stimulation of the right inferior occipital cortex, a patient with refractory epilepsy was transiently impaired at discriminating two simultaneously presented photographs of unfamiliar faces. The critical electrode contact was located in the most posterior face-selective brain area of the human brain (right "occipital face area", rOFA) as shown both by low- (ERP) and high-frequency (gamma) electrophysiological responses as well as a face localizer in fMRI. At this electrode contact, periodic visual presentation of 6 different faces by second evoked a larger electrophysiological periodic response at 6 Hz than when the same face identity was repeated at the same rate. This intracerebral EEG repetition suppression effect was markedly reduced when face stimuli were presented upside-down, a manipulation that impairs individual face discrimination. These findings provide original evidence for a causal relationship between the face-selective right inferior occipital cortex and individual face discrimination, independently of long-term memory representations. More generally, they support the functional value of electrophysiological repetition suppression effects, indicating that these effects can be used as an index of a necessary neural representation of the changing stimulus property.

[1]  E. Halgren,et al.  LOCALISED FACE PROCESSING BY THE HUMAN PREFRONTAL CORTEX: STIMULATION-EVOKED HALLUCINATIONS OF FACES , 2000, Cognitive neuropsychology.

[2]  Bruno Rossion,et al.  Understanding individual face discrimination by means of fast periodic visual stimulation , 2014, Experimental Brain Research.

[3]  L. Koessler,et al.  Focal electrical intracerebral stimulation of a face-sensitive area causes transient prosopagnosia , 2012, Neuroscience.

[4]  J. Barton.  Structure and function in acquired prosopagnosia: lessons from a series of 10 patients with brain damage. , 2008, Journal of neuropsychology.

[5]  R. Goebel,et al.  Individual faces elicit distinct response patterns in human anterior temporal cortex , 2007, Proceedings of the National Academy of Sciences.

[6]  Bruno Rossion,et al.  A steady-state visual evoked potential approach to individual face perception: Effect of inversion, contrast-reversal and temporal dynamics , 2012, NeuroImage.

[7]  A. Freire,et al.  The Face-Inversion Effect as a Deficit in the Encoding of Configural Information: Direct Evidence , 2000, Perception.

[8]  F. Mauguière,et al.  SEEG-guided thermocoagulations , 2008, Neurology.

[9]  I. Biederman,et al.  Loci of the release from fMRI adaptation for changes in facial expression, identity, and viewpoint. , 2010, Journal of vision.

[10]  Timothy J. Andrews,et al.  An image-dependent representation of familiar and unfamiliar faces in the human ventral stream , 2009, Neuropsychologia.

[11]  J. Devlin,et al.  Triple Dissociation of Faces, Bodies, and Objects in Extrastriate Cortex , 2009, Current Biology.

[12]  Marlene Behrmann,et al.  Unraveling the distributed neural code of facial identity through spatiotemporal pattern analysis , 2011, Proceedings of the National Academy of Sciences.

[13]  J. Haxby,et al.  The distributed human neural system for face perception , 2000, Trends in Cognitive Sciences.

[14]  Andrew D. Engell,et al.  The relationship of γ oscillations and face-specific ERPs recorded subdurally from occipitotemporal cortex. , 2011, Cerebral cortex.

[15]  T. Allison,et al.  Human extrastriate visual cortex and the perception of faces, words, numbers, and colors. , 1994, Cerebral cortex.

[16]  D. Regan.  Some characteristics of average steady-state and transient responses evoked by modulated light. , 1966, Electroencephalography and clinical neurophysiology.

[17]  D. Pitcher,et al.  Transcranial Magnetic Stimulation Disrupts the Perception and Embodiment of Facial Expressions , 2008, The Journal of Neuroscience.

[18]  B. Rossion,et al.  Recovery from adaptation to facial identity is larger for upright than inverted faces in the human occipito-temporal cortex , 2006, Neuropsychologia.

[19]  L. Koessler,et al.  Combined SEEG and source localisation study of temporal lobe schizencephaly and polymicrogyria , 2009, Clinical Neurophysiology.

[20]  N. Kanwisher,et al.  The Neural Basis of the Behavioral Face-Inversion Effect , 2005, Current Biology.

[21]  T. Allison,et al.  Electrophysiological studies of human face perception. III: Effects of top-down processing on face-specific potentials. , 1999, Cerebral cortex.

[22]  H. P. Op de Beeck,et al.  Representations of Facial Identity Information in the Ventral Visual Stream Investigated with Multivoxel Pattern Analyses , 2013, The Journal of Neuroscience.

[23]  Sang Chul Chong,et al.  Interaction between the electrical stimulation of a face-selective area and the perception of face stimuli , 2013, NeuroImage.

[24]  B. Rossion,et al.  ERP evidence for the speed of face categorization in the human brain: Disentangling the contribution of low-level visual cues from face perception , 2011, Vision Research.

[25]  K. Grill-Spector,et al.  fMR-adaptation: a tool for studying the functional properties of human cortical neurons. , 2001, Acta psychologica.

[26]  R. Goebel,et al.  Cerebral Cortex doi:10.1093/cercor/bhj005 Impaired Face Discrimination in Acquired Prosopagnosia Is Associated with Abnormal Response to Individual Faces in the Right Middle Fusiform Gyrus , 2005 .

[27]  Charles Pelizzari,et al.  Transient Inability to Distinguish Between Faces: Electrophysiologic Studies , 2003, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[28]  Bruno Rossion,et al.  Acquired prosopagnosia as a face-specific disorder: Ruling out the general visual similarity account , 2010, Neuropsychologia.

[29]  K. Grill-Spector,et al.  Electrical Stimulation of Human Fusiform Face-Selective Regions Distorts Face Perception , 2012, The Journal of Neuroscience.

[30]  D. Regan.  Human brain electrophysiology: Evoked potentials and evoked magnetic fields in science and medicine , 1989 .

[31]  Andrew D. Engell,et al.  Repetition suppression of face‐selective evoked and induced EEG recorded from human cortex , 2014, Human brain mapping.

[32]  G. Yovel,et al.  TMS Evidence for the Involvement of the Right Occipital Face Area in Early Face Processing , 2007, Current Biology.

[33]  R. Yin.  Looking at Upside-down Faces , 1969 .

[34]  B. Rossion.  Picture-plane inversion leads to qualitative changes of face perception. , 2008, Acta psychologica.

[35]  Seth E. Bouvier,et al.  Behavioral deficits and cortical damage loci in cerebral achromatopsia. , 2006, Cerebral cortex.

[36]  David E. J. Linden,et al.  Combining transcranial magnetic stimulation and functional imaging in cognitive brain research: possibilities and limitations , 2003, Brain Research Reviews.

[37]  M. Tarr,et al.  The Fusiform Face Area is Part of a Network that Processes Faces at the Individual Level , 2000, Journal of Cognitive Neuroscience.

[38]  A Mouraux,et al.  Across-trial averaging of event-related EEG responses and beyond. , 2008, Magnetic resonance imaging.

[39]  A. Young,et al.  Understanding the recognition of facial identity and facial expression , 2005, Nature Reviews Neuroscience.

[40]  R. Kiani,et al.  Microstimulation of inferotemporal cortex influences face categorization , 2006, Nature.

[41]  Timothy J. Andrews,et al.  Distinct representations for facial identity and changeable aspects of faces in the human temporal lobe , 2004, NeuroImage.

[42]  B. Rossion,et al.  Defining face perception areas in the human brain: A large-scale factorial fMRI face localizer analysis , 2012, Brain and Cognition.

[43]  Lily M. Solomon-Harris,et al.  TMS to the “occipital face area” affects recognition but not categorization of faces , 2013, Brain and Cognition.

[44]  J. Sergent,et al.  Functional neuroanatomy of face and object processing. A positron emission tomography study. , 1992, Brain : a journal of neurology.

[45]  David D. Cox,et al.  Untangling invariant object recognition , 2007, Trends in Cognitive Sciences.

[46]  K. Grill-Spector,et al.  Repetition and the brain: neural models of stimulus-specific effects , 2006, Trends in Cognitive Sciences.

[47]  J Sergent,et al.  Varieties of functional deficits in prosopagnosia. , 1992, Cerebral cortex.

[48]  Kalanit Grill-Spector,et al.  Sparsely-distributed organization of face and limb activations in human ventral temporal cortex , 2010, NeuroImage.

[49]  James B. Rowe,et al.  Different Neural Mechanisms within Occipitotemporal Cortex Underlie Repetition Suppression across Same and Different-Size Faces , 2012, Cerebral cortex.

[50]  A. Norcia,et al.  The 6Hz fundamental stimulation frequency rate for individual face discrimination in the right occipito-temporal cortex , 2013, Neuropsychologia.

[51]  M. Seghier,et al.  A network of occipito-temporal face-sensitive areas besides the right middle fusiform gyrus is necessary for normal face processing. , 2003, Brain : a journal of neurology.

[52]  J. Talairach,et al.  Stereotaxic Approach to Epilepsy , 1973 .

[53]  R. Malach,et al.  Sub-exemplar shape tuning in human face-related areas. , 2007, Cerebral cortex.

[54]  Rafael Malach,et al.  Perceptual shape sensitivity to upright and inverted faces is reflected in neuronal adaptation , 2010, NeuroImage.

[55]  B. Rossion,et al.  Robust sensitivity to facial identity in the right human occipito-temporal cortex as revealed by steady-state visual-evoked potentials. , 2011, Journal of vision.

[56]  Bruno Rossion,et al.  Holistic perception of the individual face is specific and necessary: Evidence from an extensive case study of acquired prosopagnosia , 2010, Neuropsychologia.