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 (mid and posterior fusiform, respectively)]. ECoG revealed a striking anatomical and functional correspondence with fMRI data where a pair of face-selective electrodes, positioned 1 cm 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.

Figure 1.

Stimulated electrodes spatially overlap face-selective ECoG and fMRI measurements on the lateral fusiform gyrus. Functional responses are shown on the patient's native anatomy. Electrodes used for EBS (1 and 2) are labeled in each image for reference. a, Spatial distribution of ECoG responses in VTC electrodes. The location of the pair of electrodes used as control EBS is indicated with white dotted circles. Each pie chart depicts the relative power for each category of stimuli across a broadband frequency range (40–160 Hz) during a time window of 100–350 ms after stimulus onset. Pie chart diameter reflects the SNR. b, fMRI activations showing higher responses to faces than nonfaces (faces > limbs, houses, cars, guitars, flowers, t > 3, voxel level) on the inflated cortical surface (left) and volume view (right; top shows zoomed region). Boundaries of retinotopic regions are indicated in blue, green, and red. IOG, Inferior occipital gyrus.

Figure 2.

Face-selective profiles of EBS electrodes across measurements. Responses from electrodes 1 and 2 are illustrated in left and right columns, respectively, of each panel. a, Band limited power analysis for faces, limbs, cars, and houses showing stimulus-locked percentage power change relative to prestimulus baseline in a time window of 0.1 to 1.1 s after stimulus onset in four standard frequency bands (rows 1–4). Data are averaged across 113–125 trials per category. Shaded regions indicate across-trial SE. Bottom row, Time course of t-values comparing broadband responses to faces vs nonfaces. Points above the dotted red line indicate when this difference is significant at p < 10⁻⁴. b, Mean ECoG ERPs to each category. c, Mean fMRI responses extracted from a 2-mm-radius gray matter ROI (illustrated in Fig. 1b) centered on the location of EBS electrodes. Data are averaged across 8 blocks per condition. Error bars indicate SD across blocks. *p < 10⁻¹¹, significantly higher responses to faces than nonfaces, t > 6.8.