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Decoding face information in time, frequency and space from direct intracranial recordings of the human brain

Tsuchiya, Naotsugu and Kawasaki, Hiroto and Oya, Hiroyuki and Howard, Matthew A., III and Adolphs, Ralph (2008) Decoding face information in time, frequency and space from direct intracranial recordings of the human brain. PLoS ONE, 3 (12). Art. No. e3892. ISSN 1932-6203. PMCID PMC2588533. https://resolver.caltech.edu/CaltechAUTHORS:TSUplosone08

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Abstract

Faces are processed by a neural system with distributed anatomical components, but the roles of these components remain unclear. A dominant theory of face perception postulates independent representations of invariant aspects of faces (e.g., identity) in ventral temporal cortex including the fusiform gyrus, and changeable aspects of faces (e.g., emotion) in lateral temporal cortex including the superior temporal sulcus. Here we recorded neuronal activity directly from the cortical surface in 9 neurosurgical subjects undergoing epilepsy monitoring while they viewed static and dynamic facial expressions. Applying novel decoding analyses to the power spectrogram of electrocorticograms (ECoG) from over 100 contacts in ventral and lateral temporal cortex, we found better representation of both invariant and changeable aspects of faces in ventral than lateral temporal cortex. Critical information for discriminating faces from geometric patterns was carried by power modulations between 50 to 150 Hz. For both static and dynamic face stimuli, we obtained a higher decoding performance in ventral than lateral temporal cortex. For discriminating fearful from happy expressions, critical information was carried by power modulation between 60–150 Hz and below 30 Hz, and again better decoded in ventral than lateral temporal cortex. Task-relevant attention improved decoding accuracy more than 10% across a wide frequency range in ventral but not at all in lateral temporal cortex. Spatial searchlight decoding showed that decoding performance was highest around the middle fusiform gyrus. Finally, we found that the right hemisphere, in general, showed superior decoding to the left hemisphere. Taken together, our results challenge the dominant model for independent face representation of invariant and changeable aspects: information about both face attributes was better decoded from a single region in the middle fusiform gyrus.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1371/journal.pone.0003892DOIArticle
http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0003892PublisherArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2588533/PubMed CentralArticle
ORCID:
AuthorORCID
Adolphs, Ralph0000-0002-8053-9692
Additional Information:© 2008 Tsuchiya et al. Received October 14, 2008; Accepted November 6, 2008; Published December 9, 2008. We thank Haiming Chen for overall technical assistance, Yota Kimura, Christopher Kovach and Joe Hitchon for their assistance during various phases of the experiment, Dirk Neumann and Ueli Rutishauser for helpful discussion on the analysis, and Alex Maier, Rufin VanRullen, Christof Koch and Fred Gosselin for their comments on the manuscript. We thank all subjects who participated in the study for their time. This work was supported by a fellowship from the Japan Society for the Promotion of Science (N.T.) and grants from NIH (R03 MH070497-01A2 to H.K.; R01 DC004290-06 to M.H.), the James S. McDonnell Foundation (R.A.) and the Gordon and Betty Moore Foundation (R.A.). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript. Conceived and designed the experiments: HK RA. Performed the experiments: HK. Analyzed the data: NT. Contributed reagents/ materials/analysis tools: NT. Wrote the paper: NT HK RA. Initial data analyses: HK. Performed anatomical localization of the electrodes: HO. Performed the neurosurgery and oversaw all recordings: MAH.
Funders:
Funding AgencyGrant Number
Japan Society for the Promotion of Science (JSPS)UNSPECIFIED
NIHR03 MH070497-01A2
NIHR01 DC004290-06
James S. McDonnell FoundationUNSPECIFIED
Gordon and Betty Moore FoundationUNSPECIFIED
Issue or Number:12
PubMed Central ID:PMC2588533
Record Number:CaltechAUTHORS:TSUplosone08
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:TSUplosone08
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:13626
Collection:CaltechAUTHORS
Deposited By: Jason Perez
Deposited On:04 Jun 2009 17:47
Last Modified:03 Oct 2019 00:41

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