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Intracranial Markers of Conscious Face Perception in Humans

Fabiano Baroni, Jochem van Kempen, Hiroto Kawasaki, Christopher K. Kovach, Hiroyuki Oya, Matthew A. Howard, Ralph Adolphs, Naotsugu Tsuchiya
doi: https://doi.org/10.1101/037234
Fabiano Baroni
1School of Psychological Sciences, Faculty of Biomedical and Psychological Sciences, Monash University, Australia
2NeuroEngineering Laboratory, Department of Electrical & Electronic Engineering, The University of Melbourne, Australia
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Jochem van Kempen
3Institute of Neuroscience, Newcastle University, Newcastle upon Tyne, United Kingdom
1School of Psychological Sciences, Faculty of Biomedical and Psychological Sciences, Monash University, Australia
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Hiroto Kawasaki
4Department of Neurosurgery, University of Iowa, Iowa City, IA, USA
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Christopher K. Kovach
4Department of Neurosurgery, University of Iowa, Iowa City, IA, USA
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Hiroyuki Oya
4Department of Neurosurgery, University of Iowa, Iowa City, IA, USA
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Matthew A. Howard
4Department of Neurosurgery, University of Iowa, Iowa City, IA, USA
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Ralph Adolphs
5Division of Humanities and Social Sciences, California Institute of Technology, Pasadena, CA, USA
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Naotsugu Tsuchiya
1School of Psychological Sciences, Faculty of Biomedical and Psychological Sciences, Monash University, Australia
6Monash Institute of Cognitive and Clinical Neuroscience, Monash University, Australia
7Decoding and Controlling Brain Information, Japan Science and Technology Agency, Chiyoda-ku, Tokyo, Japan
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Abstract

Investigations of the neuronal basis of consciousness have greatly benefited from protocols that involve the presentation of stimuli at perceptual threshold, enabling the assessment of the patterns of brain activity that correlate with conscious perception, independently of any changes in sensory input. However, the comparison between perceived and unperceived trials would be expected to isolate not only the core neuronal substrate of a particular conscious perception, but also aspects of brain activity that facilitate conscious perception, such as attention, and aspects that tend to follow perception, such as memory formation. We provide a refinement of the threshold presentation approach, by combining an analysis of the neuronal responses observed during the presentation of faces partially masked by Continuous Flash Suppression, and those responses observed during the unmasked presentation of faces and other images. We employed multidimensional classifiers to decode physical properties of stimuli or perceptual states from spectrotemporal representations of electrocorticographic signals (1071 channels in 5 subjects). The comparison between seen and unseen faces in the masked condition revealed discriminant neuronal activity in several loci in the ventral and lateral temporal cortices known to subserve face processing including the fusiform gyrus and the superior temporal sulcus. While activity in both ventral and lateral loci discriminated upright faces from other categories in the unmasked condition, with higher decoding accuracy in ventral electrodes, only ventral areas discriminated upright from inverted faces. Our results suggest a distributed network for conscious visual perception, with a prominent role for the fusiform gyrus in the configural perception of faces, and possibly other objects that can be perceived as holistic wholes. More generally, we advocate comparative analysis of neuronal recordings obtained during different, but related, experimental protocols as a promising direction towards elucidating the functional specificities of the patterns of neuronal activation that accompany our conscious experiences.

Author Summary How the brain generates conscious perception from information present at the senses is a major unsolved question in neuroscience. In humans, this question has been investigated using mostly non-invasive neuroimaging recordings such as EEG, MEG or fMRI, which each have limitations in spatial and/or temporal resolution. Here, we recorded electrocorticography (ECoG) from subdural electrodes implanted on the ventral and lateral surface of the temporal lobes in five epileptic patients undergoing pre-surgical seizure monitoring while they engaged in visual perception tasks, hence achieving excellent temporal and spatial resolution. By using a visual illusion that can dissociate the physical properties of sensory stimuli from their subjective conscious visibility, we observed neuronal responses that discriminate visible from invisible trials in response to face images in a subset of electrodes implanted on the ventral and lateral sides of the temporal lobe. To assess the face specificity of neuronal activity for each electrode in the same subjects, we also administered an unmasked visual task which comprised images of faces and other categories, which revealed that only ventral areas can discriminate upright from inverted faces. Our results suggest a prominent role of the fusiform gyrus in the conscious configural perception of faces.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted February 01, 2016.
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Intracranial Markers of Conscious Face Perception in Humans
Fabiano Baroni, Jochem van Kempen, Hiroto Kawasaki, Christopher K. Kovach, Hiroyuki Oya, Matthew A. Howard, Ralph Adolphs, Naotsugu Tsuchiya
bioRxiv 037234; doi: https://doi.org/10.1101/037234
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Intracranial Markers of Conscious Face Perception in Humans
Fabiano Baroni, Jochem van Kempen, Hiroto Kawasaki, Christopher K. Kovach, Hiroyuki Oya, Matthew A. Howard, Ralph Adolphs, Naotsugu Tsuchiya
bioRxiv 037234; doi: https://doi.org/10.1101/037234

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