Visual mechanisms for voice-identity recognition flexibly adjust to auditory noise level.

A Real-World Size Organization of Object Responses in Occipitotemporal Cortex

Simple SummaryWe showed dogs and humans live-action stimuli (actors and objects) and videos of the same stimuli during fMRI to measure the equivalency of live and two-dimensional stimuli in the dog’s brain. We found that video stimuli were effective in defining face and object regions. However, the human fusiform face area and posterior superior temporal sulcus, and the analogous area in the dog brain, appeared to respond preferentially to live stimuli. In object regions, there was not a significantly different response between live and video stimuli.Previous research to localize face areas in dogs’ brains has generally relied on static images or videos. However, most dogs do not naturally engage with two-dimensional images, raising the question of whether dogs perceive such images as representations of real faces and objects. To measure the equivalency of live and two-dimensional stimuli in the dog’s brain, during functional magnetic resonance imaging (fMRI) we presented dogs and humans with live-action stimuli (actors and objects) as well as videos of the same actors and objects. The dogs (n = 7) and humans (n = 5) were presented with 20 s blocks of faces and objects in random order. In dogs, we found significant areas of increased activation in the putative dog face area, and in humans, we found significant areas of increased activation in the fusiform face area to both live and video stimuli. In both dogs and humans, we found areas of significant activation in the posterior superior temporal sulcus (ectosylvian fissure in dogs) and the lateral occipital complex (entolateral gyrus in dogs) to both live and video stimuli. Of these regions of interest, only the area along the ectosylvian fissure in dogs showed significantly more activation to live faces than to video faces, whereas, in humans, both the fusiform face area and posterior superior temporal sulcus responded significantly more to live conditions than video conditions. However, using the video conditions alone, we were able to localize all regions of interest in both dogs and humans. Therefore, videos can be used to localize these regions of interest, though live conditions may be more salient.

Macaque neurophysiology found image-invariant representations of face identity in a face-selective patch in anterior temporal cortex. A face-selective area in human anterior temporal lobe (fATL) has been reported, but has not been reliably identified, and its function and relationship with posterior face areas is poorly understood. Here, we used fMRI adaptation and neuropsychology to ask whether fATL contains image-invariant representations of face identity, and if so, whether these representations require normal functioning of fusiform face area (FFA) and occipital face area (OFA). We first used a dynamic localizer to demonstrate that 14 of 16 normal subjects exhibit a highly selective right fATL. Next, we found evidence that this area subserves image-invariant representation of identity: Right fATL showed repetition suppression to the same identity across different images, while other areas did not. Finally, to examine fATL's relationship with posterior areas, we used the same procedures with Galen, an acquired prosopagnosic who lost right FFA and OFA. Despite the absence of posterior face areas, Galen's right fATL preserved its face selectivity and showed repetition suppression comparable to that in controls. Our findings suggest that right fATL contains image-invariant face representations that can persist despite the absence of right FFA and OFA, but these representations are not sufficient for normal face recognition.

Face specific broadband electrocorticographic spectral power change in the rhinal cortex

A quantitative link between face discrimination deficits and neuronal selectivity for faces in autism☆

Perception of faces has been shown to engage a domain-specific set of brain regions, including the occipital face area (OFA) and the fusiform face area (FFA). It is commonly held that the OFA is responsible for the detection of faces in the environment, whereas the FFA is responsible for processing the identity of the face. However, an alternative model posits that the FFA is responsible for face detection and subsequently recruits the OFA to analyze the face parts in the service of identification. An essential prediction of the former model is that the OFA is not sensitive to the arrangement of internal face parts. In the current fMRI study, we test the sensitivity of the OFA and FFA to the configuration of face parts. Participants were shown faces in which the internal parts were presented in a typical configuration (two eyes above a nose above a mouth) or in an atypical configuration (the locations of individual parts were shuffled within the face outline). Perception of the atypical faces evoked a significantly larger response than typical faces in the OFA and in a wide swath of the surrounding posterior occipitotemporal cortices. Surprisingly, typical faces did not evoke a significantly larger response than atypical faces anywhere in the brain, including the FFA (although some subthreshold differences were observed). We propose that face processing in the FFA results in inhibitory sculpting of activation in the OFA, which accounts for this region's weaker response to typical than to atypical configurations.

Body dysmorphic disorder (BDD) and anorexia nervosa (AN) are both characterized by distorted perception of appearance. Previous studies in BDD suggest abnormalities in visual processing of own and others' faces, but no study has examined visual processing of faces in AN, nor directly compared the two disorders in this respect. We collected functional magnetic resonance imaging data on 60 individuals of equivalent age and gender in each of three groups--20 BDD, 20 weight-restored AN, and 20 healthy controls (HC)--while they viewed images of others' faces that contained only high or low spatial frequency information (HSF or LSF). We tested hypotheses about functional connectivity within specialized sub-networks for HSF and LSF visual processing, using psychophysiological interaction analyses. The BDD group demonstrated increased functional connectivity compared to HC between left anterior occipital face area and right fusiform face area (FFA) for LSF faces, which was associated with symptom severity. Both BDD and AN groups had increased connectivity compared to HC between FFA and precuneous/posterior cingulate gyrus for LSF faces, and decreased connectivity between FFA and insula. In addition, we found that LSF connectivity between FFA and posterior cingulate gyrus was significantly associated with thoughts about own appearance in AN. Results suggest similar abnormal functional connectivity within higher-order systems for face processing in BDD and AN, but distinct abnormal connectivity patterns within occipito-temporal visual networks. Findings may have implications for understanding relationships between these disorders, and the pathophysiology underlying perceptual distortions.

Faces are among the most important visual stimuli we perceive, informing us not only about a person's identity, but also about their mood, sex, age and direction of gaze. The ability to extract this information within a fraction of a second of viewing a face is important for normal social interactions and has probably played a critical role in the survival of our primate ancestors. Considerable evidence from behavioural, neuropsychological and neurophysiological investigations supports the hypothesis that humans have specialized cognitive and neural mechanisms dedicated to the perception of faces (the face-specificity hypothesis). Here, we review the literature on a region of the human brain that appears to play a key role in face perception, known as the fusiform face area (FFA). Section 1 outlines the theoretical background for much of this work. The face-specificity hypothesis falls squarely on one side of a longstanding debate in the fields of cognitive science and cognitive neuroscience concerning the extent to which the mind/brain is composed of: (i) special-purpose ('domain-specific') mechanisms, each dedicated to processing a specific kind of information (e.g. faces, according to the face-specificity hypothesis), versus (ii) general-purpose ('domain-general') mechanisms, each capable of operating on any kind of information. Face perception has long served both as one of the prime candidates of a domain-specific process and as a key target for attack by proponents of domain-general theories of brain and mind. Section 2 briefly reviews the prior literature on face perception from behaviour and neurophysiology. This work supports the face-specificity hypothesis and argues against its domain-general alternatives (the individuation hypothesis, the expertise hypothesis and others). Section 3 outlines the more recent evidence on this debate from brain imaging, focusing particularly on the FFA. We review the evidence that the FFA is selectively engaged in face perception, by addressing (and rebutting) five of the most widely discussed alternatives to this hypothesis. In section 4, we consider recent findings that are beginning to provide clues into the computations conducted in the FFA and the nature of the representations the FFA extracts from faces. We argue that the FFA is engaged both in detecting faces and in extracting the necessary perceptual information to recognize them, and that the properties of the FFA mirror previously identified behavioural signatures of face-specific processing (e.g. the face-inversion effect). Section 5 asks how the computations and representations in the FFA differ from those occurring in other nearby regions of cortex that respond strongly to faces and objects. The evidence indicates clear functional dissociations between these regions, demonstrating that the FFA shows not only functional specificity but also area specificity. We end by speculating in section 6 on some of the broader questions raised by current research on the FFA, including the developmental origins of this region and the question of whether faces are unique versus whether similarly specialized mechanisms also exist for other domains of high-level perception and cognition.

This study indirectly tested the hypothesis that individuals with autism spectrum disorders (ASDs) have impaired neural connections between the amygdala, fusiform face area, and superior temporal sulcus, key processing nodes of the 'social brain'. This would be evidenced by abnormalities in the major fibre tracts known to connect these structures, including the inferior longitudinal fasciculus and inferior fronto-occipital fasciculus. Magnetic resonance diffusion tensor imaging was performed on 20 right-handed males (ASD = 10, controls = 10) with a mean age 13.5 ± 4.0 years. Subjects were group-matched according to age, full-scale IQ, handedness, and ethnicity. Fractional anisotropy was used to assess structural integrity of major fibre tracts. Voxel-wise comparison of white matter fractional anisotropy was conducted between groups using ANCOVA adjusting for age, full-scale IQ, and brain volume. Volumes of interest were identified using predetermined probability and cluster thresholds. Follow-up tractography was performed to confirm the anatomic location of all volumes of interest which were observed primarily in peri-callosal regions and the temporal lobes. The regions of lower fractional anisotropy, as confirmed by tractography, involved the inferior longitudinal fasciculus/inferior fronto-occipital fasciculus, superior longitudinal fasciculus, and corpus callosum/cingulum. Notably, some volumes of interest were adjacent to the fusiform face area, bilaterally, corresponding to involvement of the inferior longitudinal fasciculus. The largest effect sizes were noted for volumes of interest in the right anterior radiation of the corpus callosum/cingulum and right fusiform face area (inferior longitudinal fasciculus). This study provides preliminary evidence of impaired neural connectivity in the corpus callosum/cingulum and temporal lobes involving the inferior longitudinal fasciculus/inferior fronto-occipital fasciculus and superior longitudinal fasciculus in ASDs. These findings provide preliminary support for aberrant neural connectivity between the amygdala, fusiform face area, and superior temporal sulcus-temporal lobe structures critical for normal social perception and cognition.

Patterns of neural response in face regions are predicted by low-level image properties

Modeling face recognition in the predictive coding framework: A combined computational modeling and functional imaging study

Anxious individuals have a greater tendency to categorize faces with ambiguous emotional expressions as fearful (Richards et al., 2002). These behavioral findings might reflect anxiety-related biases in stimulus representation within the human amygdala. Here, we used functional magnetic resonance imaging (fMRI) together with a continuous adaptation design to investigate the representation of faces from three expression continua (surprise-fear, sadness-fear, and surprise-sadness) within the amygdala and other brain regions implicated in face processing. Fifty-four healthy adult participants completed a face expression categorization task. Nineteen of these participants also viewed the same expressions presented using type 1 index 1 sequences while fMRI data were acquired. Behavioral analyses revealed an anxiety-related categorization bias in the surprise-fear continuum alone. Here, elevated anxiety was associated with a more rapid transition from surprise to fear responses as a function of percentage fear in the face presented, leading to increased fear categorizations for faces with a mid-way blend of surprise and fear. fMRI analyses revealed that high trait anxious participants also showed greater representational similarity, as indexed by greater adaptation of the Blood Oxygenation Level Dependent (BOLD) signal, between 50/50 surprise/fear expression blends and faces from the fear end of the surprise-fear continuum in both the right amygdala and right fusiform face area (FFA). No equivalent biases were observed for the other expression continua. These findings suggest that anxiety-related biases in the processing of expressions intermediate between surprise and fear may be linked to differential representation of these stimuli in the amygdala and FFA. The absence of anxiety-related biases for the sad-fear continuum might reflect intermediate expressions from the surprise-fear continuum being most ambiguous in threat-relevance.

Choosing food is not a trivial decision that people need to make daily, which is often subject to social influences. Here, we studied a human homolog of social transmission of food preference (STFP) as observed in rodents and other animals via chemosignals of body secretions. Human social chemosignals (sweat) produced during a disgust or neutral state among a group of donors were presented to participants undergoing a 2-alternative-forced-choice food healthiness judgment task during functional magnetic resonance imaging (fMRI). Response speed and two key signal detection indices—d’ (discrimination sensitivity) and β (response bias)—converged to indicate that social chemosignals of disgust facilitated food healthiness decisions, in contrast to primary disgust elicitors (disgust odors) that impaired the judgment. fMRI analyses (disgust vs. neutral sweat) revealed that the fusiform face area (FFA), amygdala, and orbitofrontal cortex (OFC) were engaged in processing social chemosignals of disgust during food judgment. Importantly, a double contrast of social signaling across modalities (olfactory vs. visual—facial expressions) indicated that the FFA and OFC exhibited preferential response to social chemosignals of disgust. Together, our findings provide initial evidence for human STFP, where social chemosignals are incorporated into food decisions by engaging social and emotional areas of the brain.

The fusiform face area (FFA) is defined by its selectivity for faces. Several studies have shown that the response of FFA to nonface objects can predict behavioral performance for these objects. However, one possible account is that experts pay more attention to objects in their domain of expertise, driving signals up. Here, we show an effect of expertise with nonface objects in FFA that cannot be explained by differential attention to objects of expertise. We explore the relationship between cortical thickness of FFA and face and object recognition using the Cambridge Face Memory Test and Vanderbilt Expertise Test, respectively. We measured cortical thickness in functionally defined regions in a group of men who evidenced functional expertise effects for cars in FFA. Performance with faces and objects together accounted for approximately 40% of the variance in cortical thickness of several FFA patches. Whereas participants with a thicker FFA cortex performed better with vehicles, those with a thinner FFA cortex performed better with faces and living objects. The results point to a domain-general role of FFA in object perception and reveal an interesting double dissociation that does not contrast faces and objects but rather living and nonliving objects.

Viewing faces or bodies activates category-selective areas of visual cortex, including the fusiform face area (FFA), fusiform body area (FBA), and extrastriate body area (EBA). Here, using fMRI, we investigate the development of these areas, focusing on the right FFA and FBA. Despite the overlap of functionally defined FFA and FBA (54%-75% overlap), we found that these regions developed along different trajectories. With age (7-32 years old), the FFA gradually increased in size and selectivity, and was significantly larger and more face-selective in adults than children. By contrast, the size and selectivity of the FBA did not correlate with age, and were equivalent in children and adults. Whereas in adults the FFA and FBA were comparable in size, in children the FBA was on average 70% larger than the FFA. These findings suggest that, in children, the fusiform gyrus is predominantly selective for bodies, with commensurate face-selective responses apparent later in development. Moreover, differences in the development of the FFA and FBA indicate that overlapping functional brain areas, supported by the same anatomical structure, can develop along different trajectories.