A functional MRI study of face recognition in patients with prosopagnosia.

An fMRI investigation was conducted to determine whether patients with impaired face recognition, a deficit known as prosopagnosia, would show functional activation in the fusiform gyrus, the neural substrate for face processing, when viewing faces. While the patients did show activation in the fusiform gyrus, with significantly more voxels in posterior areas than their control subjects, this activation was not sufficient for face processing. In one of the patients, the posterior activation was particularly evident in the left hemisphere, which is thought to be involved in feature-based strategies of face perception. We conclude that an increased reliance on feature-based processing in prosopagnosia leads to a recruitment of neurons in posterior regions of the fusiform gyrus, regions that are not ideally suited for processing faces.     

Natural and manufactured objects activate the fusiform face area

Recent fMRI studies indicate that the anterior fusiform gyrus (the fusiform face area, FFA) is specialized for face recognition. However, the analyses used to determine face selectivity have not ruled out the possibility that other object categories produce significant activation in the FFA, relative to baseline. In the current fMRI study, we use a conservative hypothesis testing approach to show that FFA activation is not selective for faces. Rather, the FFA response is almost completely explained by a graded response in which faces produce more activation than either manufactured or natural objects, but those categories produce a statistically greater response than the baseline task. These findings question whether the FFA can be interpreted as a specialized module for face recognition.     

Neural correlates of personally familiar faces: parents, partner and own faces

Investigations of the neural correlates of face recognition have typically used old/new paradigms where subjects learn to recognize new faces or identify famous faces. Familiar faces, however, include one's own face, partner's and parents' faces. Using event-related fMRI, we examined the neural correlates of these personally familiar faces. Ten participants were presented with photographs of own, partner, parents, famous and unfamiliar faces and responded to a distinct target. Whole brain, two regions of interest (fusiform gyrus and cingulate gyrus), and multiple linear regression analyses were conducted. Compared with baseline, all familiar faces activated the fusiform gyrus; own faces also activated occipital regions and the precuneus; partner faces activated similar areas, but in addition, the parahippocampal gyrus, middle superior temporal gyri and middle frontal gyrus. Compared with unfamiliar faces, only personally familiar faces activated the cingulate gyrus and the extent of activation varied with face category. Partner faces also activated the insula, amygdala and thalamus. Regions of interest analyses and laterality indices showed anatomical distinctions of processing the personally familiar faces within the fusiform and cingulate gyri. Famous faces were right lateralized whereas personally familiar faces, particularly partner and own faces, elicited bilateral activations. Regression analyses show experiential predictors modulated with neural activity related to own and partner faces. Thus, personally familiar faces activated the core visual areas and extended frontal regions, related to semantic and person knowledge and the extent and areas of activation varied with face type.     

Emotional attention in acquired prosopagnosia

The present study investigated whether emotionally expressive faces guide attention and modulate fMRI activity in fusiform gyrus in acquired prosopagnosia. Patient PS, a pure case of acquired prosopagnosia with intact right middle fusiform gyrus, performed two behavioral experiments and a functional imaging experiment to address these questions. In a visual search task involving face stimuli, PS was faster to select the target face when it was expressing fear or happiness as compared to when it was emotionally neutral. In a change detection task, PS detected significantly more changes when the changed face was fearful as compared to when it was neutral. Finally, an fMRI experiment showed enhanced activation to emotionally expressive faces and bodies in right fusiform gyrus. In addition, PS showed normal body-selective activation in right fusiform gyrus, partially overlapping the fusiform face area. Together these behavioral and neuroimaging results show that attention was preferentially allocated to emotional faces in patient PS, as observed in healthy subjects. We conclude that systems involved in the emotional guidance of attention by facial expression can function normally in acquired prosopagnosia, and can thus be dissociated from systems involved in face identification.     

Congenital prosopagnosia: multistage anatomical and functional deficits in face processing circuitry

Face recognition is a primary social skill which depends on a distributed neural network. A pronounced face recognition deficit in the absence of any lesion is seen in congenital prosopagnosia. This study investigating 24 congenital prosopagnosic subjects and 25 control subjects aims at elucidating its neural basis with fMRI and voxel-based morphometry. We found a comprehensive behavioral pattern, an impairment in visual recognition for faces and buildings that spared long-term memory for faces with negative valence. Anatomical analysis revealed diminished gray matter density in the bilateral lingual gyrus, the right middle temporal gyrus, and the dorsolateral prefrontal cortex. In most of these areas, gray matter density correlated with memory success. Decreased functional activation was found in the left fusiform gyrus, a crucial area for face processing, and in the dorsolateral prefrontal cortex, whereas activation of the medial prefrontal cortex was enhanced. Hence, our data lend strength to the hypothesis that congenital prosopagnosia is explained by network dysfunction and suggest that anatomic curtailing of visual processing in the lingual gyrus plays a substantial role. The dysfunctional circuitry further encompasses the fusiform gyrus and the dorsolateral prefrontal cortex, which may contribute to their difficulties in long-term memory for complex visual information. Despite their deficits in face identity recognition, processing of emotion related information is preserved and possibly mediated by the medial prefrontal cortex. Congenital prosopagnosia may, therefore, be a blueprint of differential curtailing in networks of visual cognition.     

The involvement of the "fusiform face area" in processing facial expression

We conducted an fMRI investigation to test the widely accepted notion that the fusiform face area (FFA) mediates the processing of facial identity but not expression. Participants attended either to the identity or to the expression of the same set of faces. If the processing of identity is neuroanatomically dissociable from that of expression, then one might expect the FFA to show higher activation when processing identity as opposed to expression. Contrary to this prediction, the FFA showed higher activation for judgments of expression. Furthermore, the FFA was sensitive to variations in expression even when attention was directed to identity. Finally, an independent observation showed higher activation in the FFA for passive viewing of faces when expression was varied as compared to when it remained constant. These findings suggest an interactive network for the processing of expression and identity, in which information about expression is computed from the unique structure of individual faces.     

The Role of Face Familiarity in Eye Tracking of Faces by Individuals with Autism Spectrum Disorders

It has been shown that individuals with autism spectrum disorders (ASD) demonstrate normal activation in the fusiform gyrus when viewing familiar, but not unfamiliar faces. The current study utilized eye tracking to investigate patterns of attention underlying familiar versus unfamiliar face processing in ASD. Eye movements of 18 typically developing participants and 17 individuals with ASD were recorded while passively viewing three face categories: unfamiliar non-repeating faces, a repeating highly familiar face, and a repeating previously unfamiliar face. Results suggest that individuals with ASD do not exhibit more normative gaze patterns when viewing familiar faces. A second task assessed facial recognition accuracy and response time for familiar and novel faces. The groups did not differ on accuracy or reaction times.     

fMRI activation of the fusiform gyrus and amygdala to cartoon characters but not to faces in a boy with autism

Abnormal hypoactivation in the amygdala and fusiform gyrus, brain areas that participate in face processing and social cognition, has consistently been demonstrated in persons with autism. We investigated activity in these areas in a boy with autism, DD, who had a special interest in "Digimon" cartoon characters. DD individuates Digimon faster than familiar faces and objects, but he individuates familiar faces no faster than objects. In contrast, a typically developing boy with an interest in "Pokemon" cartoon characters is equally fast at individuating faces and Pokemon and faster at individuating faces and Pokemon than objects and Digimon. In addition, using functional magnetic resonance imaging (fMRI), we show that DD activates his amygdala and fusiform gyrus for perceptual discriminations involving Digimon but not for those involving familiar or unfamiliar faces. This pattern of activation is not seen in the typically developing control with an interest in Pokemon or in a second comparison case who has autism but no interest in Digimon. These results have important implications for our understanding of autism, cortical face specialization, and the possible role of the amygdala in the development of perceptual expertise.     

Recovery from adaptation to facial identity is larger for upright than inverted faces in the human occipito-temporal cortex

Human faces look more similar to each other when they are presented upside-down, leading to an increase of error rates and response times during individual face discrimination tasks. Here we used functional magnetic resonance imaging (fMRI) to test the hypothesis that this perceived similarity leads to a lower recovery from identity adaptation for inverted faces than for upright faces in face-sensitive areas of the occipito-temporal cortex. Ten subjects were presented with blocks of upright and inverted faces, with the same face identity repeated consecutively in half of the blocks, and different facial identities repeated in the other blocks. When face stimuli were presented upright, the percent signal change in the bilateral middle fusiform gyrus (MFG) was larger for different faces as compared to same faces, replicating previous observations of a recovery from facial identity adaptation in this region. However, there was no significant recovery from adaptation when different inverted faces were presented. Most interestingly, the difference in activation between upright and inverted faces increased progressively during a block when different facial identities were presented. A similar pattern of activation was found in the left middle fusiform gyrus, but was less clear-cut in bilateral face-sensitive areas of the inferior occipital cortex. These findings show that the differential level of activation to upright and inverted faces in the fusiform gyrus is mainly due to a difference in recovery from adaptation, and they explain the discrepancies in the results reported in previous fMRI studies which compared the processing of upright and inverted faces. The lack of recovery from adaptation for inverted faces in the fusiform gyrus may underlie the face inversion effect (FIE), which takes place during perceptual encoding of individual face representations.     

Being BOLD: The neural dynamics of face perception

According to a non‐hierarchical view of human cortical face processing, selective responses to faces may emerge in a higher‐order area of the hierarchy, in the lateral part of the middle fusiform gyrus (fusiform face area [FFA]) independently from face‐selective responses in the lateral inferior occipital gyrus (occipital face area [OFA]), a lower order area. Here we provide a stringent test of this hypothesis by gradually revealing segmented face stimuli throughout strict linear descrambling of phase information [Ales et al., 2012]. Using a short sampling rate (500 ms) of fMRI acquisition and single subject statistical analysis, we show a face‐selective responses emerging earlier, that is, at a lower level of structural (i.e., phase) information, in the FFA compared with the OFA. In both regions, a face detection response emerging at a lower level of structural information for upright than inverted faces, both in the FFA and OFA, in line with behavioral responses and with previous findings of delayed responses to inverted faces with direct recordings of neural activity were also reported. Overall, these results support the non‐hierarchical view of human cortical face processing and open new perspectives for time‐resolved analysis at the single subject level of fMRI data obtained during continuously evolving visual stimulation. Hum Brain Mapp 38:120–139, 2017. © 2016 Wiley Periodicals, Inc.     

Progressively analogous evidence of covert face recognition from functional magnetic resonance imaging and skin conductance responses studies involving a patient with dissociative amnesia

This is a case study involving a female patient (NN) with complete loss of autobiographical memory and identity despite normal neurological assessment. To test the hypothesis that patients with dissociative amnesia (DA) possess the ability to covertly process facial identities they are unaware of, we conducted functional magnetic resonance imaging (fMRI) and assessed skin conductance responses (SCR) to (a) strangers, (b) celebrities, and (c) familiar faces not seen since the onset of DA. We also performed associative face‐name memory tasks to test the patient's ability to learn and recall newly learned face‐name pairs. Although NN did not recognize any of the faces of her friends and relatives, their images triggered a stronger involvement of the left fusiform gyrus, the bilateral hippocampus/amygdala region, the orbitofrontal cortex, the middle temporal regions, and the precuneus, along with higher SCR. During recollection of previously learned face‐name pairs, NN (compared to healthy controls) demonstrated a weaker involvement of the hippocampus. Our findings suggest that, in DA, specific arousal systems remain capable of being activated by familiar faces outside of conscious awareness. The decreased activation observed in the hippocampus demonstrates that the functioning of memory‐sensitive regions may be impaired by trauma.     

The relationship between repetition suppression and face perception

Repetition of identical face stimuli leads to fMRI response attenuation (fMRI adaptation, fMRIa) in the core face-selective occipito-temporal visual cortical network, involving the bilateral fusiform face area (FFA) and the occipital face area (OFA). However, the functional relevance of fMRIa observed in these regions is unclear as of today. Therefore, here we aimed at investigating the relationship between fMRIa and face perception ability by measuring in the same human participants both the repetition-induced reduction of fMRI responses and identity discrimination performance outside the scanner for upright and inverted face stimuli. In the correlation analysis, the behavioral and fMRI results for the inverted faces were used as covariates to control for the individual differences in overall object perception ability and basic visual feature adaptation processes, respectively. The results revealed a significant positive correlation between the participants’ identity discrimination performance and the strength of fMRIa in the core face processing network, but not in the extrastriate body area (EBA). Furthermore, we found a strong correlation of the fMRIa between OFA and FFA and also between OFA and EBA, but not between FFA and EBA. These findings suggest that there is a face-selective component of the repetition-induced reduction of fMRI responses within the core face processing network, which reflects functionally relevant adaptation processes involved in face identity perception.     

Prosopagnosia following nonconvulsive status epilepticus associated with a left fusiform gyrus malformation

A 67-year-old, right-handed woman became unable to recognize familiar faces following a period of nonconvulsive status epilepticus. Neuropsychological assessment revealed a relatively selective impairment of familiar face recognition in the absence of low-level visual deficits or widespread cognitive impairment. MRI scanning demonstrated an isolated lesion, probably a venous angioma, involving the left fusiform gyrus, mirror-symmetrical to the site typically linked to prosopagnosia. Potential explanations for the patient's prosopagnosia include seizure-related damage to a left fusiform region required for fully competent face recognition and damage to the contralateral fusiform gyrus via interhemispheric connections. Focal neuropsychological deficits in patients with refractory partial epilepsy who develop nonconvulsive status epilepticus may be underdiagnosed.     

Neural correlates of processing facial identity based on features versus their spacing

Adults' expertise in recognizing facial identity involves encoding subtle differences among faces in the shape of individual facial features (featural processing) and in the spacing among features (a type of configural processing called sensitivity to second-order relations). We used fMRI to investigate the neural mechanisms that differentiate these two types of processing. Participants made same/different judgments about pairs of faces that differed only in the shape of the eyes and mouth, with minimal differences in spacing (featural blocks), or pairs of faces that had identical features but differed in the positions of those features (spacing blocks). From a localizer scan with faces, objects, and houses, we identified regions with comparatively more activity for faces, including the fusiform face area (FFA) in the right fusiform gyrus, other extrastriate regions, and prefrontal cortices. Contrasts between the featural and spacing conditions revealed distributed patterns of activity differentiating the two conditions. A region of the right fusiform gyrus (near but not overlapping the localized FFA) showed greater activity during the spacing task, along with multiple areas of right frontal cortex, whereas left prefrontal activity increased for featural processing. These patterns of activity were not related to differences in performance between the two tasks. The results indicate that the processing of facial features is distinct from the processing of second-order relations in faces, and that these functions are mediated by separate and lateralized networks involving the right fusiform gyrus, although the FFA as defined from a localizer scan is not differentially involved.     

Face perception is mediated by a distributed cortical network

The neural system associated with face perception in the human brain was investigated using functional magnetic resonance imaging (fMRI). In contrast to many studies that focused on discreet face-responsive regions, the objective of the current study was to demonstrate that regardless of stimulus format, emotional valence, or task demands, face perception evokes activation in a distributed cortical network. Subjects viewed various stimuli (line drawings of unfamiliar faces and photographs of unfamiliar, famous, and emotional faces) and their phase scrambled versions. A network of face-responsive regions was identified that included the inferior occipital gyrus, fusiform gyrus, superior temporal sulcus, hippocampus, amygdala, inferior frontal gyrus, and orbitofrontal cortex. Although bilateral activation was found in all regions, the response in the right hemisphere was stronger. This hemispheric asymmetry was manifested by larger and more significant clusters of activation and larger number of subjects who showed the effect. A region of interest analysis revealed that while all face stimuli evoked activation within all regions, viewing famous and emotional faces resulted in larger spatial extents of activation and higher amplitudes of the fMRI signal. These results indicate that a mere percept of a face is sufficient to localize activation within the distributed cortical network that mediates the visual analysis of facial identity and expression.     

Neural substrates for functionally discriminating self-face from personally familiar faces

Understanding the neurobiological substrates of self-recognition yields important insight into socially and clinically critical cognitive functions such as theory of mind. Experimental evidence suggests that right frontal and parietal lobes preferentially process self-referent information. Recognition of one's own face is an important parameter of self-recognition, but well-controlled experimental data on the brain substrates of self-face recognition is limited. The goal of this study was to characterize the activation specific to self-face in comparison with control conditions of two levels of familiarity: unknown unfamiliar face and the more stringent control of a personally familiar face. We studied 12 healthy volunteers who made "unknown," "familiar," and "self" judgments about photographs of three types of faces: six different novel faces, a personally familiar face (participant's fraternity brother), and their own face during an event-related functional MRI (fMRI) experiment. Contrasting unknown faces with baseline showed activation of the inferior occipital lobe, which supports previous findings suggesting the presence of a generalized face-processing area within the inferior occipital-temporal region. Activation in response to a familiar face, when contrasted with an unknown face, invoked insula, middle temporal, inferior parietal, and medial frontal lobe activation, which is consistent with an existing hypothesis suggesting familiar face recognition taps neural substrates that are different from those involved in general facial processing. Brain response to self-face, when contrasted with familiar face, revealed activation in the right superior frontal gyrus, medial frontal and inferior parietal lobes, and left middle temporal gyrus. The contrast familiar vs. self produced activation only in the anterior cingulate gyrus. Our results support the existence of a bilateral network for both perceptual and executive aspects of self-face processing that cannot be accounted for by a simple hemispheric dominance model. This network is similar to those implicated in social cognition, mirror neuron matching, and face-name matching. Our findings also show that some regions of the medial frontal and parietal lobes are specifically activated by familiar faces but not unknown or self-faces, indicating that these regions may serve as markers of face familiarity and that the differences between activation associated with self-face recognition and familiar face recognition are subtle and appear to be localized to lateral frontal, parietal, and temporal regions.     

Preserved function of the fusiform face area in schizophrenia as revealed by fMRI

Many lines of evidence suggest that individuals with schizophrenia suffer from face processing deficits. However, the specificity of these deficits and the neural dysfunction underlying them remain unclear. To address these questions, we evaluated the functional status of a critical region for face processing, the fusiform face area (FFA), in subjects with schizophrenia. Fourteen schizophrenia patients and 10 healthy control subjects participated in an fMRI experiment to determine the functional status of the FFA by viewing a series of faces and exemplars of other object categories, while completing a low-level task designed to verify their engagement with the stimuli. Behavioral performance and activation of the FFA were equivalent between groups. Thirteen of 14 patients and all control subjects displayed FFA activation. Furthermore, the degree of FFA activation, as measured by FFA volume and magnitude of activity, was similar between groups. The FFA, a critical region in the neural system subserving the perceptual processing of faces, appears to be intact in schizophrenia. These results call into question the presence of a specific face processing deficit in schizophrenia.     

Preserved function of the fusiform face area in schizophrenia as revealed by fMRI

Many lines of evidence suggest that individuals with schizophrenia suffer from face processing deficits. However, the specificity of these deficits and the neural dysfunction underlying them remain unclear. To address these questions, we evaluated the functional status of a critical region for face processing, the fusiform face area (FFA), in subjects with schizophrenia. Fourteen schizophrenia patients and 10 healthy control subjects participated in an fMRI experiment to determine the functional status of the FFA by viewing a series of faces and exemplars of other object categories, while completing a low-level task designed to verify their engagement with the stimuli. Behavioral performance and activation of the FFA were equivalent between groups. Thirteen of 14 patients and all control subjects displayed FFA activation. Furthermore, the degree of FFA activation, as measured by FFA volume and magnitude of activity, was similar between groups. The FFA, a critical region in the neural system subserving the perceptual processing of faces, appears to be intact in schizophrenia. These results call into question the presence of a specific face processing deficit in schizophrenia.     

Different fusiform activity to stranger and personally familiar faces in shy and social adults

Abstract

Although shyness is associated with deficits in different aspects of face processing including face recognition and facial emotions, we know relatively little about the neural correlates of face processing among individuals who are shy. Here we show reduced activation to stranger faces among shy adults in a key brain area involved in face processing. Event-related functional magnetic resonance imaging scans were acquired on 12 shy and 12 social young adults during the rapid presentation of stranger and personally familiar neutral faces. Shy adults exhibited significantly less bilateral activation in the fusiform face area (FFA) in response to stranger faces and significantly greater bilateral activation in the same region to personally familiar faces than their social counterparts. Shy adults also exhibited significantly greater right amygdala activation in response to stranger faces than social adults. Among social adults, stranger faces elicited greater FFA activation than personally familiar faces. Findings suggest that there are distinct patterns of neural activation in the FFA in response to viewing stranger and personally familiar faces among shy and social adults.