Electrical Stimulation of Human Fusiform Face-Selective Regions Distorts Face Perception

Abstract

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.

Mapping human temporal and parietal neuronal population activity and functional coupling during mathematical cognition

“…The HFB classifiers also were the only ones with classification accuracy significantly above chance in every subject [permutation test, P < 0.05, false-discovery rate (FDR) corrected]. These findings corroborate previous work showing a high correspondence between HFB activity and local neuronal firing rate and with fMRI blood-oxygen level-dependent activity (42)(43)(44)(45)(46)(47). Because selectivity for the different stimulus classes/trial types was most prominent in the HFB band, we focused on HFB activity in subsequent analyses.…”

“…In subsequent analyses, based on task 2, we focused on pITG math sites that included the NFA sites. Also of note, the number/math-selective region described above is anatomically distinct from other category-selective regions within the VTC, such as the fusiform face area (FFA) (46) and the word form area (WFA), sites that responded selectively to letters in task 1 and/or to written memory statements in task 2 (Fig. S3).…”

Neurons in the human amygdala selective for perceived emotion

“…Microstimulation of inferotemporal cortex in monkeys (45) and electrical brain stimulation in fusiform areas in humans (46) have suggested a causal role of the temporal cortex in face categorization and perception. Future studies using direct stimulation of the amygdala will be important to further determine the nature of its contribution to the subjective perception of facial emotion.…”

Mapping human brain networks with cortico-cortical evoked potentials

“…Recently, optogenetics have allowed the selective stimulation of neuronal subtypes in localized regions of animal brains [40] and assessing the effects of that stimulation on functional neural networks [41]. With the increasing use of research protocols to study effects of cortical stimulation in patients implanted with invasive electrodes for epilepsy monitoring, there has been recent resurgence of interest into the effects of cortical stimulation upon behaviour and perception [26,[42][43][44]. While most of the aforementioned work focused on the link between stimulation and changes in perception or behaviour (e.g.…”