Face-selective neural responses in the human fusiform gyrus have been widely examined. However, their causal role in human face perception is largely unknown. Here, we used a multimodal approach of electrocorticography (ECoG), high-resolution functional magnetic resonance imaging (fMRI), and electrical brain stimulation (EBS) to directly investigate the causal role of face-selective neural responses of the fusiform gyrus (FG) in face perception in a patient implanted with subdural electrodes in the right inferior temporal lobe. High-resolution fMRI identified two distinct FG face-selective regions (mFus-faces and pFus-faces). ECoG revealed a striking anatomical and functional correspondence with fMRI data where a pair of face-selective electrodes, positioned one centimeter apart, overlapped mFus-faces and pFus-faces, respectively. Moreover, electrical charge delivered to this pair of electrodes induced a profound face-specific perceptual distortion during viewing of real faces. Specifically, the subject reported a “metamorphosed” appearance of faces of people in the room. Several controls illustrate the specificity of the effect to the perception of faces. EBS of mFus-faces and pFus-faces neither produced a significant deficit in naming pictures of famous faces on the computer, nor did it affect the appearance of nonface objects. Further, the appearance of faces remained unaffected during both sham stimulation and stimulation of a pair of nearby electrodes that were not face-selective. Overall, our findings reveal a striking convergence of fMRI, ECoG, and EBS, which together offer a rare causal link between functional subsets of the human FG network and face perception.

Summary Background Activity in the living human brain can be studied using multiple methods, spanning a wide range of spatial and temporal resolutions. We investigated the relationship between electric field potentials measured with electrocorticography (ECoG) and the blood oxygenation level dependent (BOLD) response measured with functional magnetic resonance imaging (fMRI). We set out to explain the full set of measurements by modeling the underlying neural circuits. Results ECoG responses in visual cortex can be separated into two visually driven components. One component is a specific temporal response that follows each stimulus contrast reversal (“stimulus locked”); the other component is an increase in the response variance (“asynchronous”). For electrodes in visual cortex (V1, V2, V3), the two measures respond to stimuli in the same region of visual space, but they have different spatial summation properties. The stimulus-locked ECoG component sums contrast approximately linearly across space; spatial summation in the asynchronous ECoG component is sub-additive. Spatial summation measured using BOLD closely matches the asynchronous component. We created a neural simulation that accurately captures the main features of the ECoG time series; in the simulation the stimulus-locked and asynchronous components arise from different neural circuits. Conclusions These observations suggest that the two ECoG components arise from different neural sources within the same cortical region. The spatial summation measurements and simulations suggest that the BOLD response arises primarily from neural sources that generate asynchronous broadband ECoG component.

Is there a distinct area within the human visual system that has a preferential response to numerals, as there is for faces, words, or scenes? We addressed this question using intracranial electrophysiological recordings and observed a significantly higher response in the high-frequency broadband range (high γ, 65–150 Hz) to visually presented numerals, compared with morphologically similar (i.e., letters and false fonts) or semantically and phonologically similar stimuli (i.e., number words and non-number words). Anatomically, this preferential response was consistently localized in the inferior temporal gyrus and anterior to the temporo-occipital incisure. This region lies within or close to the fMRI signal-dropout zone produced by the nearby auditory canal and venous sinus artifacts, an observation that may account for negative findings in previous fMRI studies of preferential response to numerals. Because visual numerals are culturally dependent symbols that are only learned through education, our novel finding of anatomically localized preferential response to such symbols provides a new example of acquired category-specific responses in the human visual system.

Neuroimaging and electrophysiological studies across species have confirmed bilateral face-selective responses in the ventral temporal cortex (VTC) and prosopagnosia is reported in patients with lesions in the VTC including the fusiform gyrus (FG). As imaging and electrophysiological studies provide correlative evidence, and brain lesions often comprise both white and gray matter structures beyond the FG, we designed the current study to explore the link between face-related electrophysiological responses in the FG and the causal effects of electrical stimulation of the left or right FG in face perception. We used a combination of electrocorticography (ECoG) and electrical brain stimulation (EBS) in 10 human subjects implanted with intracranial electrodes in either the left (5 participants, 30 FG sites) or right (5 participants, 26 FG sites) hemispheres. We identified FG sites with face-selective ECoG responses, and recorded perceptual reports during EBS of these sites. In line with existing literature, face-selective ECoG responses were present in both left and right FG sites. However, when the same sites were stimulated, we observed a striking difference between hemispheres. Only EBS of the right FG caused changes in the conscious perception of faces, whereas EBS of strongly face-selective regions in the left FG produced non-facerelated visual changes, such as phosphenes. This study examines the relationship between correlative versus causal nature of ECoG and EBS, respectively, and provides important insight into the differential roles of the right versus left FG in conscious face perception.

Highlights d Visual cortical prosthetic stimulation paradigms were examined d Letters or other shapes were traced on the surface of cortex with electrical current d Static stimulation was unable to produce letter percepts in participants d Dynamic current steering evoked percepts of letter forms by blind and sighted participants