A face-selective ventral occipito-temporal map of the human brain with intracerebral potentials

Abstract

Human neuroimaging studies have identified a network of distinct face-selective regions in the ventral occipito-temporal cortex (VOTC), with a right hemispheric dominance. To date, there is no evidence for this hemispheric and regional specialization with direct measures of brain activity. To address this gap in knowledge, we recorded local neurophysiological activity from 1,678 contact electrodes implanted in the VOTC of a large group of epileptic patients (n = 28). They were presented with natural images of objects at a rapid fixed rate (six images per second: 6 Hz), with faces interleaved as every fifth stimulus (i.e., 1.2 Hz). High signal-to-noise ratio face-selective responses were objectively (i.e., exactly at the face stimulation frequency) identified and quantified throughout the whole VOTC. Face-selective responses were widely distributed across the whole VOTC, but also spatially clustered in specific regions. Among these regions, the lateral section of the right middle fusiform gyrus showed the largest face-selective response by far, offering, to our knowledge, the first supporting evidence of two decades of neuroimaging observations with direct neural measures. In addition, three distinct regions with a high proportion of face-selective responses were disclosed in the right ventral anterior temporal lobe, a region that is undersampled in neuroimaging because of magnetic susceptibility artifacts. A high proportion of contacts responding only to faces (i.e., "face-exclusive" responses) were found in these regions, suggesting that they contain populations of neurons involved in dedicated face-processing functions. Overall, these observations provide a comprehensive mapping of visual category selectivity in the whole human VOTC with direct neural measures.

Keywords: face perception; face selectivity; fast periodic visual stimulation; fusiform gyrus; intracerebral recordings.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.

FPVS and SEEG methods. (A) The FPVS paradigm. Images of objects were presented by sinusoidal contrast modulation at a rate of six stimuli per second (6 Hz). In the periodic condition shown here, a different face image was presented every five stimuli (i.e., appearing at the frequency of 6/5 = 1.2 Hz). (B) Representative examples of natural face images used in the study (actual images not shown for copyright reasons). Faces were embedded in their natural backgrounds and varied in size, viewpoint, and lighting conditions (50 face exemplars were used in total). (C) Schematic representation of the typical trajectories of depth electrodes (SEEG) implanted in the right VOTC. Intracerebral electrodes consist of 8–15 contiguous recording contacts spread along the electrode length, along the medio-lateral axis. Typical trajectories of electrodes are represented as arrays of red rectangles on schematic coronal slices (with Talairach y coordinates indicated below slices). Electrodes penetrate both gyral and sulcal cortical tissues. a, anterior; CS, calcarine sulcus; lat, lateral; LG, lingual gyrus; med, medial; PHG, parahippocampal gyrus.

Fig. 2.

Objective and high-SNR intracerebral responses in the VOTC. iEEG frequency-domain responses recorded at an individual recording contact (raw FFT amplitude) located in the right latFG (participant 14) are shown. The location of the recording contact (indicated by a red arrow) is shown using a postoperative CT coregistered to a preoperative MRI. (A) In the periodic condition, significant face-selective responses exactly at the face-selective frequency (1.2 Hz) and harmonics (up to 10.8 Hz) were observed. Note the high SNR of these responses (i.e., high amplitude at the specific frequency compared with the neighboring frequency bins), despite the brief recording time (two sequences of 70 s here). (B) In the nonperiodic condition, no face-selective responses were observed. In both conditions, general visual responses occurring exactly at the base frequency (6 Hz) and harmonics were recorded, with comparable amplitudes and SNR across conditions. *z > 3.1; P < 0.001.

Fig. 3.

Spatial distribution of face-selective contacts in the MNI space (ventral view). (A) Map of all 1,678 VOTC recording contacts across the 28 individual brains displayed in the MNI space using a transparent reconstructed cortical surface of the Colin27 brain. Each circle represents a single contact. Colored circles correspond to face-selective contacts color-coded according to their face-selective response amplitude. White-filled circles correspond to contacts that are not face-selective. For visualization purposes, individual contacts are displayed larger than their actual size (2 mm in length). (B) Examples of four individual participant hemispheres. Anatomical labels of the face-selective clusters in each participant are derived from the individual native anatomy.

Fig. 4.

Face-selective responses in distinct anatomical VOTC regions. iEEG SNR frequency spectra in each region of the right hemisphere averaged across all face-selective contacts located in the same region. SNR is computed by comparing amplitude at the frequency bin of interest to amplitude at neighboring bins (i.e., SNR = 1, no signal above noise level). The schematic locations of each region are shown on a reconstructed cortical surface of the Colin27 brain. For simplicity, regions are depicted over the cortical surface although responses were recorded within the cortex. Note the particularly large (i.e., high SNR) face-selective response recorded in the latFG and to a lesser extent in the IOG compared with other regions. Although face-selective contacts were found in the right antMTG/ITG (Fig. 8A), no clear responses were visible on the averaged spectrum, which is therefore not shown. Note that we did not record in the most posterior (in the OCC) and anterior parts of the FG.

Fig. S1.

Spatial distribution of face-selective, visually responsive, and nonresponsive contacts in the MNI space (ventral view). (A) Map of all 1,678 VOTC recording contacts across the group of 28 participants displayed in the MNI space using a transparent reconstructed cortical surface of the Colin27 brain. Each circle represents a single contact. Face-selective contacts (red) are represented along with contacts visually responsive to the base frequency but not face-selective (blue) and nonresponsive contacts (white, no face-selective or general visual responses recorded). The number of recorded contacts was higher in the left than in the right hemisphere (988 vs. 690). (B) Face-selective contacts in the MNI space colored according to their anatomical label in the individual anatomy.

Fig. S2.

Schematic representation of the parcellation scheme used to determine the anatomical label of each face-selective contact. Anatomical regions were defined in each individual hemisphere according to major anatomical landmarks. The ventral temporal sulci [CoS, OTS, and midfusiform sulcus (MFS)] serve as medial/lateral borders of regions, whereas two coronal reference planes containing anatomical landmarks [posterior tip of the HIP and anterior tip of the parieto-occipital sulcus (POS)] serve as an anterior/posterior boundary for each region. The anatomical location of each face-selective contact was determined in the individual brain according to this anatomical subdivision and contacts were grouped by anatomical location across all participants. The schematic locations of these anatomical structures are shown on a reconstructed cortical surface of the Colin27 brain.

Fig. S3.

Averaged iEEG frequency spectra in each region of the left hemisphere. IEEG frequency spectra in each region of the left hemisphere averaged across all face-selective contacts located in the same region are shown.

Fig. 5.

Example of face-selective responses in three distinct anatomical regions of ventral ATL. (A) Face-selective responses recorded from the right antCoS, antOTS, and antFG in a single brain (participant 16). Note that in the antCoS and antOTS, no general visual responses were recorded at 6 Hz and harmonics (face-exclusive responses; see also Fig. 8A). *z > 3.1; P < 0.001. (B) Anatomical locations of corresponding recording contacts on MRI slices. Contacts are shown as red dots on axial (Left) and coronal (Right) slices. Electrode contacts 1, 2, and 3 are respectively located in the antCoS, antOTS, and antFG. The antFG is located between the antCoS and antOTS, at a level where the HIP is visible on a coronal slice.

Fig. 6.

Quantification of the response amplitudes in each region. Face-selective (Upper) and general visual (Lower) responses were quantified in each region as the average of the response amplitudes across contacts. The average across contacts for each region is shown separately for the left and right hemispheres. Error bars represent the SEM across contacts.

Fig. S4.

Control analyses and experiments. (A) The pattern of response amplitudes is independent from the number of harmonics included in the quantification. Although the number of harmonics included to quantify the responses was objectively defined (from the first until the highest significant harmonic across participants), the pattern of results is stable whatever the number of harmonics included in the analyses. Here face-selective responses (Upper) and general visual responses (Lower) are quantified as a function of the number of harmonics included in the analyses. Data are represented as the mean across contacts for each VOTC region (SEMs across contacts are represented as error bars). Differences between regions already emerge from the first harmonics and remain stable regardless of the number of face or base frequency harmonics used in the analyses. (B) The decrease of the general visual response in anterior regions does not result from an inability of these anterior regions to generate a response at 6 Hz. The figure compares the mean baseline-subtracted amplitude of general visual responses in the 1.5-Hz experiment (control experiment) to the general visual responses in the 6-Hz experiment (main experiment) in the 11 patients who performed both experiments. The same pattern of response amplitude in the 6- and 1.5-Hz base rate experiments are found, with a decrease of amplitudes from posterior to anterior regions. (C) The decrease of the general visual response in anterior regions is not due to a global response amplitude reduction. The mean baseline-subtracted amplitude of the general visual responses is compared across regions for groups of contacts showing similar mean face-selective response amplitudes. To do so, the following analysis was performed: (i) contacts from left and right regions were grouped together; (ii) in each region, contacts for which the face-selective response amplitude was located between 0 and 15 µV were selected (based on the range of the response of the least responsive region: antMTG/ITG): the minimum number of contacts within this amplitude range across regions was 7 in antFG; (iii) for each region a combination of 7 contacts (by randomly sampling from the pool of contacts in the range of 0–15 µV) for which the mean amplitude was the closest to the mean amplitude of the region with the least number of contacts (i.e., antFG: 7 contacts) was searched for; and (iv) the mean general visual response amplitude at corresponding contacts was extracted. A similar reduction of general visual responses from posterior to anterior regions as for the main analysis with all of the contacts was observed.

Fig. S5.

Quantification of mean face-selective and general visual responses in each region after artifact rejection. The average across contacts for each region is shown separately for the left and right hemispheres. Error bars represent the SEM across contacts. For the artifact rejection procedure, see SI Text.

Fig. 7.

Clustered organization of face selectivity within each region. (A) Proportion of electrodes showing highly face-selective contacts in each region. (B) Mean distance between highly face-selective contacts in electrodes highlighted in A. Error bars represent the SEM. These distances were significantly smaller than when randomly shuffling the locations of contacts on the electrodes (95% lower confidence interval indicated by horizontal lines). (C) Spatial variation of face-selective response amplitude in each region. All electrodes containing at least one face-selective contact were identified and pooled across hemispheres. The number of electrodes included in the analysis for each region is indicated in parentheses. Next, electrodes were spatially centered with respect to the contact recording the largest face-selective response. Each electrode was then folded around the maximum by averaging responses from equidistant contacts on both sides of the maximum. Face-selective responses measured at corresponding contacts across electrodes were then averaged by region. The resulting profiles represent the mean variation of face-selective response amplitude as a function of the distance from the maximum (maximum located at 0 mm). To statistically assess the clustering of highly face-selective responses in each region, these profiles were compared with a random distribution of profiles generated by repeatedly performing the exact same analysis after randomly shuffling the location of contacts in each electrode (i.e., both original and random profiles were spatially centered on the largest face-selective response). Shaded gray areas and thin gray lines, respectively, represent the 95% confidence interval and the mean of these random distributions. Face-selective responses above or equal to the 95% confidence interval are shown as larger filled markers.

Fig. 8.

Face-exclusive responses. (A) Examples of recordings in single participants in right and left ATL regions. *z > 3.1; P < 0.001. (B) Proportion of face-exclusive contacts. The proportion of face-exclusive contacts (with respect to all face-selective contacts) is displayed for the three main regions (OCC, PTL, and ATL). *P < 0.05 (Pearson's χ2 test).

Fig. S6.

Average across images in each category (faces and 14 categories including cats, dogs, horses, birds, flowers, fruits, vegetables, houseplants, phones, chairs, cameras, dishes, guitars, and lamps). n indicates the number of images for each category in our set of stimuli.