Human Ventral Occipito-temporal Cortex Research Articles

Dissociated face- and word-selective intracerebral responses in the human ventral occipito-temporal cortex

The extent to which faces and written words share neural circuitry in the human brain is actively debated. Here, we compare face-selective and word-selective responses in a large group of patients (N = 37) implanted with intracerebral electrodes in the ventral occipito-temporal cortex (VOTC). Both face-selective (i.e., significantly different responses to faces vs. non-face visual objects) and word-selective (i.e., significantly different responses to words vs. pseudofonts) neural activity is isolated with frequency-tagging. Critically, this sensitive approach allows to objectively quantify category-selective neural responses and disentangle them from general visual responses. About 70% of significant electrode contacts show either face-selectivity or word-selectivity only, with the expected right and left hemispheric dominance, respectively. Spatial dissociations are also found within core regions of face and word processing, with a medio-lateral dissociation in the fusiform gyrus (FG) and surrounding sulci, respectively. In the 30% of overlapping face- and word-selective contacts across the VOTC or in the FG and surrounding sulci, between-category-selective amplitudes (faces vs. words) show no-to-weak correlations, despite strong correlations in both the within-category-selective amplitudes (face–face, word–word) and the general visual responses to words and faces. Overall, these observations support the view that category-selective circuitry for faces and written words is largely dissociated in the human adult VOTC.

Dissociated face- and word-selective intracerebral responses in the human ventral occipito-temporal cortex

The extent to which faces and written words share neural circuitry in the human brain is actively debated. We provide an original contribution to this debate by comparing face-selective and word-selective responses in a large group of patients (N=37) implanted with intracerebral electrodes in the ventral occipito-temporal cortex (VOTC). Both face-selective (i.e., significantly different responses to faces vs. nonface objects) and word-selective (i.e., significantly different responses to words vs. pseudofonts) neural activity is isolated through frequency-tagging (Jonas et al., 2016; Lochy et al., 2018, respectively). Critically, this approach allows disentangling category-selective neural responses from general visual responses. Overall, we find that 69.26% of significant contacts show either face- or word-selectivity, with the expected right and left hemispheric dominance, respectively (Fig.1A,B). Moreover, the center of mass for word-contacts is more lateral than for face-contacts, with no differences in postero-anterior axis (Fig.2A). Spatial dissociations are also found within core regions of face and word processing, with a medio-lateral dissociation in the fusiform gyrus (FG) and surrounding sulci (FG+sulci;Fig.2B), while a postero-anterior dissociation is found in the inferior occipital gyrus (IOG;Fig.2C). Despite their spatial dissociations in the FG+sulci and IOG, most overlap in category-selective responses is found in these regions (Fig.1C). Critically, in the overlap-contacts, across the whole brain or specifically in the FG+sulci, between-category (word-face) selective-amplitudes showed no-to-weak correlations, despite strong correlations for within-category (face-face, word-word) selective-amplitudes (Fig.3A), and a strong correlation in non-selective general-amplitudes to words-faces. Moreover, substantial overlap and no-to-weak correlations were observed between faces and a control category (houses) known to be functionally dissociated from faces. Overall, we conclude that category-selectivity for faces and words is largely dissociated in the human VOTC, with a limited spatial overlap likely due to the distant recording of dissociated populations of neurons rather than to shared category-selective representations.

The neural basis of rapid unfamiliar face individuation with human intracerebral recordings

Rapid individuation of conspecifics’ faces is ecologically important in the human species, whether the face belongs to a familiar or unfamiliar individual. Here we tested a large group (N = 69) of epileptic patients implanted with intracerebral electrodes throughout the ventral occipito-temporal cortex (VOTC). We used a frequency-tagging visual stimulation paradigm optimized to objectively measure face individuation with direct neural recordings. This enabled providing an extensive map of the significantly larger neural responses to upright than to inverted unfamiliar faces, i.e. reflecting visual face individuation processes that go beyond physical image differences. These high-level face individuation responses are both distributed and anatomically confined to a strip of cortex running from the inferior occipital gyrus all along the lateral fusiform gyrus, with a large right hemispheric dominance. Importantly, face individuation responses are limited anteriorly to the bilateral anterior fusiform gyrus and surrounding sulci, with a near absence of significant responses in the extensively sampled temporal pole. This large-scale mapping provides original evidence that face individuation is supported by a distributed yet anatomically constrained population of neurons in the human VOTC, and highlights the importance of probing this function with face stimuli devoid of associated semantic, verbal and affective information.

Spatially Dissociated Intracerebral Maps for Face- and House-Selective Activity in the Human Ventral Occipito-Temporal Cortex.

We report a comprehensive mapping of the human ventral occipito-temporal cortex (VOTC) for selective responses to frequency-tagged faces or landmarks (houses) presented in rapid periodic trains of objects, with intracerebral recordings in a large sample (N = 75). Face-selective contacts are three times more numerous than house-selective contacts and show a larger amplitude, with a right hemisphere advantage for faces. Most importantly, these category-selective contacts are spatially dissociated along the lateral-to-medial VOTC axis, respectively, consistent with neuroimaging evidence. At the minority of "overlap" contacts responding selectively to both faces and houses, response amplitude to the two categories is not correlated, suggesting a contribution of distinct populations of neurons responding selectively to each category. The medio-lateral dissociation also extends into the underexplored anterior temporal lobe (ATL). In this region, a relatively high number of intracerebral recording contacts show category-exclusive responses (i.e., without any response to baseline visual objects) to faces but rarely to houses, in line with the proposed role of this region in processing people-related semantic information. Altogether, these observations shed novel insight on the neural basis of human visual recognition and strengthen the validity of the frequency-tagging approach coupled with intracerebral recordings in epileptic patients to understand human brain function.

Word selectivity in high-level visual cortex and reading skill

Word-selective neural responses in human ventral occipito-temporal cortex (VOTC) emerge as children learn to read, creating a visual word form area (VWFA) in the literate brain. It has been suggested that the VWFA arises through competition between pre-existing selectivity for other stimulus categories, changing the topography of VOTC to support rapid word recognition. Here, we hypothesized that competition between words and objects would be resolved as children acquire reading skill. Using functional magnetic resonance imaging (fMRI), we examined the relationship between responses to words and objects in VOTC in two ways. First, we defined the VWFA using a words > objects contrast and found that only skilled readers had a region that responded more to words than objects. Second, we defined the VWFA using a words > faces contrast and examined selectivity for words over objects in this region. We found that word selectivity strongly correlated with reading skill, suggesting reading skill-dependent tuning for words. Furthermore, we found that low word selectivity in struggling readers was not due to a lack of response to words, but to a high response to objects. Our results suggest that the fine-tuning of word-selective responses in VOTC is a critical component of skilled reading.

Selective visual representation of letters and words in the left ventral occipito-temporal cortex with intracerebral recordings

We report a comprehensive cartography of selective responses to visual letters and words in the human ventral occipito-temporal cortex (VOTC) with direct neural recordings, clarifying key aspects of the neural basis of reading. Intracerebral recordings were performed in a large group of patients (n = 37) presented with visual words inserted periodically in rapid sequences of pseudofonts, nonwords, or pseudowords, enabling classification of responses at three levels of word processing: letter, prelexical, and lexical. While letter-selective responses are found in much of the VOTC, with a higher proportion in left posterior regions, prelexical/lexical responses are confined to the middle and anterior sections of the left fusiform gyrus. This region overlaps with and extends more anteriorly than the visual word form area typically identified with functional magnetic resonance imaging. In this region, prelexical responses provide evidence for populations of neurons sensitive to the statistical regularity of letter combinations independently of lexical responses to familiar words. Despite extensive sampling in anterior ventral temporal regions, there is no hierarchical organization between prelexical and lexical responses in the left fusiform gyrus. Overall, distinct word processing levels depend on neural populations that are spatially intermingled rather than organized according to a strict postero-anterior hierarchy in the left VOTC.

The Fusiform and Occipital Face Areas Can Process a Nonface Category Equivalently to Faces.

The fusiform and occipital face areas (FFA and OFA) are functionally defined brain regions in human ventral occipitotemporal cortex associated with face perception. There is an ongoing debate, however, whether these regions are face-specific or whether they also facilitate the perception of nonface object categories. Here, we present evidence that, under certain conditions, bilateral FFA and OFA respond to a nonface category equivalently to faces. In two fMRI sessions, participants performed same-different judgments on two object categories (faces and chairs). In one session, participants differentiated between distinct exemplars of each category, and in the other session, participants differentiated between exemplars that differed only in the shape or spatial configuration of their features (featural/configural differences). During the latter session, the within-category similarity was comparable for both object categories. When differentiating between distinct exemplars of each category, bilateral FFA and OFA responded more strongly to faces than to chairs. In contrast, during featural/configural difference judgments, bilateral FFA and OFA responded equivalently to both object categories. Importantly, during featural/configural difference judgments, the magnitude of activity within FFA and OFA evoked by the chair task predicted the participants' behavioral performance. In contrast, when participants differentiated between distinct chair exemplars, activity within these face regions did not predict the behavioral performance of the chair task. We conclude that, when the within-category similarity of a face and a nonface category is comparable and when the same cognitive strategies used to process a face are applied to a nonface category, the FFA and OFA respond equivalently to that nonface category and faces.

Mapping face categorization in the human ventral occipitotemporal cortex with direct neural intracranial recordings.

The neural basis of face categorization has been widely investigated with functional magnetic resonance imaging (fMRI), identifying a set of face-selective local regions in the ventral occipitotemporal cortex (VOTC). However, indirect recording of neural activity with fMRI is associated with large fluctuations of signal across regions, often underestimating face-selective responses in the anterior VOTC. While direct recording of neural activity with subdural grids of electrodes (electrocorticography, ECoG) or depth electrodes (stereotactic electroencephalography, SEEG) offers a unique opportunity to fill this gap in knowledge, these studies rather reveal widely distributed face-selective responses. Moreover, intracranial recordings are complicated by interindividual variability in neuroanatomy, ambiguity in definition, and quantification of responses of interest, as well as limited access to sulci with ECoG. Here, we propose to combine SEEG in large samples of individuals with fast periodic visual stimulation to objectively define, quantify, and characterize face categorization across the whole VOTC. This approach reconciles the wide distribution of neural face categorization responses with their (right) hemispheric and regional specialization, and reveals several face-selective regions in anterior VOTC sulci. We outline the challenges of this research program to understand the neural basis of face categorization and high-level visual recognition in general.

Preferential coding of eye/hand motor actions in the human ventral occipito-temporal cortex

The human ventral occipito-temporal cortex (OTC) contains areas specialized for particular perceptual/semantic categories, such as faces (fusiform face area, FFA) and places (parahippocampal place area, PPA). This organization has been interpreted as reflecting the visual structure of the world, i.e. perceptual similarity and/or eccentricity biases. However, recent functional magnetic resonance imaging (fMRI) studies have shown not only that regions of the OTC are modulated by non-visual, action-related object properties but also by motor planning and execution, although the functional role and specificity of this motor-related activity are still unclear. Here, through a reanalysis of previously published data, we tested whether the selectivity for perceptual/semantic categories in the OTC corresponds to a preference for particular motor actions. The results demonstrate for the first time that face- and place-selective regions of the OTC exhibit preferential BOLD response to the execution of hand pointing and saccadic eye movements, respectively. Moreover, multivariate analyses provide novel evidence for the consistency across neural representations of stimulus category and movement effector in OTC. According to a ‘spatial hypothesis’, this pattern of results originates from the match between the region eccentricity bias and the typical action space of the motor effectors. Alternatively, the double dissociation may be caused by the different effect produced by hand vs. eye movements on regions coding for body representation. Overall, the present findings offer novel insights on the coupling between visual and motor cortical representations.

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

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.

Relative sensitivity to low- vs. high-level visual properties in face-sensitive regions of the human ventral occipito-temporal cortex: evidence from intra-cerebral recordings

Neuroimaging studies have identified a network of regions in the human ventral occipito-temporal cortex (VOTC) sensitive to faces. Using intra-cerebral electrophysiological recordings, we compared the relative responsivity of the different regions to face-structure using a periodic visual stimulation paradigm. Recordings were made in 17 epileptic patients implanted with linear-array depth-electrodes (>1000 contacts in the VOTC). In Experiment 1, we presented sequences of phase-scrambled and intact face stimuli (equalised for low-level image properties) alternating at a fixed frequency of 3Hz (6 images/s) while patients completed an orthogonal task. Significant periodic EEG responses (SSVEPs) reflecting high-level face structure processing were found at 3 Hz, while responses reflecting low-level visual processing (e.g. local contrast change) were recorded at 6 Hz. An index of high-level processing (3Hz/(3Hz+6Hz)) showed a posterior-to-anterior gradient, reflecting increased sensitivity to face structure going from the occipital to the temporo-polar cortex, with a right hemisphere lateralisation. In Experiment 2, we further investigated face structure processing with a sweep VEP paradigm (Ales et al., 2012; 4/17 patients). Stimulation was similar to Experiment 1 except the visibility (phase coherence) of the face image was parametrically varied so that a face gradually emerged over the course of a sequence. The patients performed a face detection task during the trials. Responses at 3Hz, objective markers of face detection, were found in all patients on contacts in the lateral fusiform gyrus and inferior occipital gyrus that overlapped with those defined in Experiment 1. All regions showed non-linear voltage vs coherence functions at 3Hz, with thresholds lying around ≈40% coherence. Sites in the lateral fusiform gyrus had a distinct step-like response profile suggestive of categorical face detection. These findings demonstrate that face-sensitive regions are organised with a posterior-to-anterior gradient of increasingly selective high-level visual processing. These regions appear to detect face structure in a non-linear/categorical manner. Meeting abstract presented at VSS 2015.

Functional connectivity constrains the category-related organization of human ventral occipitotemporal cortex.

One of the most robust and oft-replicated findings in cognitive neuroscience is that several spatially distinct, functionally dissociable ventral occipitotemporal cortex (VOTC) regions respond preferentially to different categories of concrete entities. However, the determinants of this category-related organization remain to be fully determined. One recent proposal is that privileged connectivity of these VOTC regions with other regions that store and/or process category-relevant properties may be a major contributing factor. To test this hypothesis, we used a multicategory functional magnetic resonance imaging (MRI) localizer to individually define category-related brain regions of interest (ROIs) in a large group of subjects (n = 33). We then used these ROIs in resting-state functional connectivity MRI analyses to explore spontaneous functional connectivity among these regions. We demonstrate that during rest, distinct category-preferential VOTC regions show differentially stronger functional connectivity with other regions that have congruent category-preference, as defined by the functional localizer. Importantly, a "tool"-preferential region in the left medial fusiform gyrus showed differentially stronger functional connectivity with other left lateralized cortical regions associated with perceiving and knowing about common tools-posterior middle temporal gyrus (involved in perception of nonbiological motion), lateral parietal cortex (critical for reaching, grasping, manipulating), and ventral premotor cortex (involved in storing/executing motor programs)-relative to other category-related regions in VOTC of both the right and left hemisphere. Our findings support the claim that privileged connectivity with other cortical regions that store and/or process category-relevant properties constrains the category-related organization of VOTC.

Level of discrimination as an organizing principle in the human ventral occipito-temporal cortex for object recognition

Level of discrimination as an organizing principle in the human ventral occipito-temporal cortex for object recognition

Alternating Zones Selective to Faces and Written Words in the Human Ventral Occipitotemporal Cortex

Recognition of faces and written words is associated with category-specific brain activation in the ventral occipitotemporal cortex (vOT). However, topological and functional relationships between face-selective and word-selective vOT regions remain unclear. In this study, we collected data from patients with intractable epilepsy who underwent high-density recording of surface field potentials in the vOT. "Faces" and "letterstrings" induced outstanding category-selective responses among the 24 visual categories tested, particularly in high-γ band powers. Strikingly, within-hemispheric analysis revealed alternation of face-selective and letterstring-selective zones within the vOT. Two distinct face-selective zones located anterior and posterior portions of the mid-fusiform sulcus whereas letterstring-selective zones alternated between and outside of these 2 face-selective zones. Further, a classification analysis indicated that activity patterns of these zones mostly represent dedicated categories. Functional connectivity analysis using Granger causality indicated asymmetrically directed causal influences from face-selective to letterstring-selective regions. These results challenge the prevailing view that different categories are represented in distinct contiguous regions in the vOT.

Individual Variability in Location Impacts Orthographic Selectivity in the "Visual Word Form Area"

Strong evidence exists for a key role of the human ventral occipitotemporal cortex (vOT) in reading, yet there have been conflicting reports about the specificity of this area in orthographic versus nonorthographic processing. We suggest that the inconsistencies in the literature can be explained by the method used to identify regions that respond to words. Here we provide evidence that the "visual word form area" (VWFA) shows word selectivity when identified at the individual subject level, but that intersubject variability in the location and size of the VWFA causes this selectivity to be washed out if defining the VWFA at the group level or based on coordinates from the literature. Our findings confirm the existence of a word-selective region in vOT while providing an explanation for why other studies have found a lack of word specificity in vOT.

Focal electrical intracerebral stimulation of a face-sensitive area causes transient prosopagnosia

Face perception is subtended by a large set of areas in the human ventral occipito-temporal cortex. However, the role of these areas and their importance for face recognition remain largely unclear. Here we report a case of transient selective impairment in face recognition (prosopagnosia) induced by focal electrical intracerebral stimulation of the right inferior occipital gyrus. This area presents with typical face-sensitivity as evidenced by functional neuroimaging right occipital face area (OFA). A face-sensitive intracerebral N170 was also recorded in this area, supporting its contribution as a source of the well-known N170 component typically recorded on the scalp. Altogether, these observations indicate that face recognition can be selectively impaired by local disruption of a single face-sensitive area of the network subtending this function, the right OFA.

Defining face perception areas in the human brain: A large-scale factorial fMRI face localizer analysis

A number of human brain areas showing a larger response to faces than to objects from different categories, or to scrambled faces, have been identified in neuroimaging studies. Depending on the statistical criteria used, the set of areas can be overextended or minimized, both at the local (size of areas) and global (number of areas) levels. Here we analyzed a whole-brain factorial functional localizer obtained in a large sample of right-handed participants (40). Faces (F), objects (O; cars) and their phase-scrambled counterparts (SF, SO) were presented in a block design during a one-back task that was well matched for difficulty across conditions. A conjunction contrast at the group level {(F–SF) and (F–O)} identified six clusters: in the pulvinar, inferior occipital gyrus (so-called OFA), middle fusiform gyrus (so-called FFA), posterior superior temporal sulcus, amygdala, and anterior infero-temporal cortex, which were all strongly right lateralized. While the FFA showed the largest difference between faces and cars, it also showed the least face-selective response, responding more to cars than scrambled cars. Moreover, the FFA’s larger response to scrambled faces than scrambled cars suggests that its face-sensitivity is partly due to low-level visual cues. In contrast, the pattern of activation in the OFA points to a higher degree of face-selectivity. A BOLD latency mapping analysis suggests that face-sensitivity emerges first in the right FFA, as compared to all other areas. Individual brain analyses support these observations, but also highlight the large amount of interindividual variability in terms of number, height, extent and localization of the areas responding preferentially to faces in the human ventral occipito-temporal cortex. This observation emphasizes the need to rely on different statistical thresholds across the whole brain and across individuals to define these areas, but also raises some concerns regarding any objective labeling of these areas to make them correspond across individual brains. This large-scale analysis helps understanding the set of face-sensitive areas in the human brain, and encourages in-depth single participant analyses in which the whole set of areas is considered in each individual brain.

Hemispheric differences of color responses in human ventral visual cortex

INTRODUCTION. Human ventral occipito-temporal cortex (VOT) has been shown to contain several visual field maps involved in the color and shape processing pathways (Brewer et al., 2005; Arcaro and Kastner, 2007). Patient lesion studies indicate that there may be hemispheric differences in the pathways subserving color vision and word form recognition. Here we compare the organization of the color responses between hemispheres in human ventral visual cortex.

Selective Attention Modulates Face-Specific Induced Gamma Oscillations Recorded from Ventral Occipitotemporal Cortex

EEG studies from subdural electrodes have demonstrated a face-specific event-related potential (face-N200) recorded from human ventral occipitotemporal cortex. The insensitivity of face-N200 to task manipulations has supported the proposal that face-N200 reflects an initial obligatory response to faces. This result stands in striking contrast to results of neuroimaging studies that have demonstrated strong task sensitivity of the fusiform hemodynamic response evoked by faces, and thus has created a paradox in the face perception literature. We recorded field potentials directly from the cortical surface of 16 patients while they selectively attended to faces or houses. Here we report that face-specific gamma activity recorded at face-N200 sites is strongly modulated by selective attention, while face-N200 is not. Our results reconcile prior electrophysiological and hemodynamic studies of face perception, and suggest that attentional modulation of the face response follows an initial phase that is largely insensitive to attention.