Fast temporal dynamics and causal relevance of face processing in the human temporal cortex

Abstract

Recordings with a large number of intracranial electrodes in eight neurosurgical subjects offered a unique opportunity to examine the fast temporal dynamics of face processing simultaneously across a relatively large extent of the human temporal cortex (TC). Measuring the power of slow oscillatory bands of activity ({theta}, , {beta}, and {gamma}) as well as High-Frequency Broadband (HFB, 70-177 Hz) signal, we found that the HFB showed the strongest univariate and multivariate changes in response to face compared to non-face stimuli. Using the HFB signal as a surrogate marker for local cortical engagement, we identified recording sites with selective responses to faces that were anatomically consistent across subjects and responded with graded strength to human, mammal, bird, and marine animal faces. Importantly, the most face selective sites were located more posteriorly and responded earlier than those with less selective responses to faces. Using machine learning based methods, we demonstrated that a sparse model focusing on information from the human face selective sites performed as well as, or better than, anatomically distributed models of face processing when discriminating faces from non-faces stimuli. Lastly, we identified the posterior fusiform (pFUS) site as causally the most relevant node for inducing distortion of face perception by direct electrical stimulation. Our findings support the notion of face information being processed first in the most selective sites - that are anatomically discrete and localizable within individual brains and anatomically consistent across subjects - which is then distributed in time to less selective anterior temporal sites within a time window that is too fast to be detected by current neuroimaging methods. The new information about the fast spatio-temporal dynamics of face processing across multiple sites of the human brain provides a new common ground for unifying the seemingly contradictory modular and distributed models of face processing in the human brain.