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.
Project description:Functional magnetic resonance imaging (fMRI) has identified face- and body part-selective regions, as well as distributed activation patterns for object categories across human ventral temporal cortex (VTC), eliciting a debate regarding functional organization in VTC and neural coding of object categories. Using high-resolution fMRI, we illustrate that face- and limb-selective activations alternate in a series of largely nonoverlapping clusters in lateral VTC along the inferior occipital gyrus (IOG), fusiform gyrus (FG), and occipito-temporal sulcus (OTS). Both general linear model (GLM) and multivoxel pattern (MVP) analyses show that face- and limb-selective activations minimally overlap and that this organization is consistent across experiments and days. We provide a reliable method to separate two face-selective clusters on the middle and posterior FG (mFus and pFus), and another on the IOG using their spatial relation to limb-selective activations and retinotopic areas hV4, VO-1/2, and hMT+. Furthermore, these activations show a gradient of increasing face selectivity and decreasing limb selectivity from the IOG to the mFus. Finally, MVP analyses indicate that there is differential information for faces in lateral VTC (containing weakly- and highly-selective voxels) relative to non-selective voxels in medial VTC. These findings suggest a sparsely-distributed organization where sparseness refers to the presence of several face- and limb-selective clusters in VTC, and distributed refers to the presence of different amounts of information in highly-, weakly-, and non-selective voxels. Consequently, theories of object recognition should consider the functional and spatial constraints of neural coding across a series of minimally overlapping category-selective clusters that are themselves distributed.
Project description:Functional localizers are particularly prevalent in functional magnetic resonance imaging (fMRI) studies concerning face processing. In this study, we extend the knowledge on face localizers regarding four important aspects: First, activation differences in occipital and fusiform face areas (OFA/FFA) and amygdala are characterized by increased activation while precuneus and medial prefrontal cortex show decreased deactivation to faces versus control stimuli. The face-selective posterior superior temporal sulcus is a hybrid area exhibiting increased activation within its inferior and decreased deactivation within its superior part. Second, the employed control stimuli can impact on whether a region is classified in group analyses as face-selective or not. We specifically investigated this for recently described cytoarchitectonic subregions of the fusiform cortex (FG-2/FG-4). Averaged activity across voxels in FG-4 was stronger for faces than objects, houses, or landscapes. In FG-2, averaged activity was only significantly stronger in comparison with landscapes, but small peaks within this area were detected for comparison versus objects and houses. Third, reproducibility of individual peak activations is excellent for right FFA and quite good for right OFA, whereas within all other areas it was too low to provide valid information on time-invariant individual peaks. Finally, the fine-grained spatial activation patterns in right OFA and FFA are both time-invariant within each individual and sufficiently different between individuals to enable identification of individual participants with near-perfect precision (fMRI fingerprinting).
Project description:Regions of the occipital and temporal lobes, including a region in the fusiform gyrus (FG), have been proposed to constitute a "core" visual representation system for faces, in part because they show face selectivity and face repetition suppression. But recent fMRI studies of developmental prosopagnosics (DPs) raise questions about whether these measures relate to face processing skills. Although DPs manifest deficient face processing, most studies to date have not shown unequivocal reductions of functional responses in the proposed core regions. We scanned 15 DPs and 15 non-DP control participants with fMRI while employing factor analysis to derive behavioral components related to face identification or other processes. Repetition suppression specific to facial identities in FG or to expression in FG and STS did not show compelling relationships with face identification ability. However, we identified robust relationships between face selectivity and face identification ability in FG across our sample for several convergent measures, including voxel-wise statistical parametric mapping, peak face selectivity in individually defined "fusiform face areas" (FFAs), and anatomical extents (cluster sizes) of those FFAs. None of these measures showed associations with behavioral expression or object recognition ability. As a group, DPs had reduced face-selective responses in bilateral FFA when compared with non-DPs. Individual DPs were also more likely than non-DPs to lack expected face-selective activity in core regions. These findings associate individual differences in face processing ability with selectivity in core face processing regions. This confirms that face selectivity can provide a valid marker for neural mechanisms that contribute to face identification ability.
Project description:We measured the fast temporal dynamics of face processing simultaneously across the human temporal cortex (TC) using intracranial recordings in eight participants. We found sites with selective responses to faces clustered in the ventral TC, which responded increasingly strongly to marine animal, bird, mammal, and human faces. Both face-selective and face-active but non-selective sites showed a posterior to anterior gradient in response time and selectivity. A sparse model focusing on information from the human face-selective sites performed as well as, or better than, anatomically distributed models when discriminating faces from non-faces stimuli. Additionally, we identified the posterior fusiform site (pFUS) as causally the most relevant node for inducing distortion of conscious face processing by direct electrical stimulation. These findings support anatomically discrete but temporally distributed response profiles in the human brain and provide a new common ground for unifying the seemingly contradictory modular and distributed modes of face processing.
Project description:Women typically remember more female than male faces, whereas men do not show a reliable own-gender bias. However, little is known about the neural correlates of this own-gender bias in face recognition memory. Using functional magnetic resonance imaging (fMRI), we investigated whether face gender modulated brain activity in fusiform and inferior occipital gyri during incidental encoding of faces. Fifteen women and 14 men underwent fMRI while passively viewing female and male faces, followed by a surprise face recognition task. Women recognized more female than male faces and showed higher activity to female than male faces in individually defined regions of fusiform and inferior occipital gyri. In contrast, men's recognition memory and blood-oxygen-level-dependent response were not modulated by face gender. Importantly, higher activity in the left fusiform gyrus (FFG) to one gender was related to better memory performance for that gender. These findings suggest that the FFG is involved in the gender bias in memory for faces, which may be linked to differential experience with female and male faces.
Project description:The fusiform face area responds selectively to faces and is causally involved in face perception. How does face-selectivity in the fusiform arise in development, and why does it develop so systematically in the same location across individuals? Preferential cortical responses to faces develop early in infancy, yet evidence is conflicting on the central question of whether visual experience with faces is necessary. Here, we revisit this question by scanning congenitally blind individuals with fMRI while they haptically explored 3D-printed faces and other stimuli. We found robust face-selective responses in the lateral fusiform gyrus of individual blind participants during haptic exploration of stimuli, indicating that neither visual experience with faces nor fovea-biased inputs is necessary for face-selectivity to arise in the lateral fusiform gyrus. Our results instead suggest a role for long-range connectivity in specifying the location of face-selectivity in the human brain.
Project description:The human face communicates a wealth of socially relevant information such as person identity, emotion, and intention. A consistent behavioral finding in autism spectrum disorder (ASD) is reduced attention to or difficulty drawing meaning from faces. However, neuroimaging research into the neural correlates of face processing differences in ASD has returned mixed results. While many studies find hypo-activation or hypo-connectivity of core and extended face network regions, others show hyper-activation, equal activation, or even activation shifted to object-selective fusiform gyrus (FG) regions in ASD during face processing. This study consolidates two decades of literature to reveal common and consistent patterns of brain activation when viewing human faces in ASD. It also addresses whether face processing in ASD is routinely shifted to object-centric regions of the FG. To do so, we conducted an extensive search of the neuroimaging literature according to PRISMA guidelines. Peak activation coordinates from a final set of 23 studies, yielding a sample of 713 participants (338 ASD), were included for quantitative meta-analysis using Activation Likelihood Estimation (ALE). ASD within-group results across studies revealed a single activation cluster in the left FG, which presented laterally to the mid-fusiform sulcus (MFS). Typically developing groups displayed common activations across core and extended face network regions. Exploratory analysis of between group findings from the literature did not yield significant results. Overall, our results suggest that individuals with ASD consistently activate at least one typical face network region, the left FG, when processing faces and this activation is not routinely shifted to object-centric areas of the FG.
Project description:Increasing evidence suggests that primate visual cortex has a specialized architecture for processing discrete object categories such as faces. Human fMRI studies have described a localized region in the fusiform gyrus [the fusiform face area (FFA)] that responds selectively to faces. In contrast, in nonhuman primates, electrophysiological and fMRI studies have instead revealed 2 apparently analogous regions of face representation: the posterior temporal face patch (PTFP) and the anterior temporal face patch (ATFP). An earlier study suggested that human FFA is homologous to the PTFP in macaque. However, in humans, no obvious homologue of the macaque ATFP has been demonstrated. Here, we used fMRI to map face-selective sites in both humans and macaques, based on equivalent stimuli in a quantitative topographic comparison. This fMRI evidence suggests that such a face-selective area exists in human anterior inferotemporal cortex, comprising the apparent homologue of the fMRI-defined ATFP in macaques.
Project description:While decades of research have demonstrated that a region of the right fusiform gyrus (FG) responds selectively to faces, a second line of research suggests that the FG responds to a range of animacy cues, including biological motion and goal-directed actions, even in the absence of faces or other human-like surface features. These findings raise the question of whether the FG is indeed sensitive to faces or to the more abstract category of animate agents. The current study uses fMRI to examine whether the FG responds to all faces in a category-specific way or whether the FG is especially sensitive to the faces of animate agents. Animate agents are defined here as intentional agents with the capacity for rational goal-directed actions. Specifically, we examine how the FG responds to an entity that looks like an animate agent but that lacks the capacity for goal-directed rational action. Region-of-interest analyses reveal that the FG activates more strongly to the animate compared with the inanimate entity, even though the surface features of both animate and inanimate entities were identical. These results suggest that the FG does not respond to all faces in a category-specific way, and is instead especially sensitive to whether an entity is animate.