Neural basis of the retrieval of people's names: evidence from brain-damaged patients and fMRI

The aim of this study was to identify the neuroanatomical basis of the retrieval of people's names. Lesion data showed that patients with language-dominant temporal lobectomy had impairments in their ability to retrieve familiar and newly learned people's names, whereas patients with language-nondominant temporal lobectomy had difficulty retrieving newly learned people's names. Functional magnetic resonance imaging experiments revealed activations in the left temporal polar region during the retrieval of familiar and newly learned people's names, and in the right superior temporal and bilateral prefrontal cortices during the retrieval of newly learned information from face cues. These data provide new evidence that the left anterior temporal region is crucial for the retrieval of people's names irrespective of their familiarity and that the right superior temporal and bilateral prefrontal areas are crucial for the process of associating newly learned people's faces and names.     

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.     

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.     

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.     

Dissociable neural responses in the hippocampus to the retrieval of facial identity and emotion: an event-related fMRI study

In studies with brain-damaged patients and experimental animals, the medial temporal lobe, including the hippocampus and parahippocampal gyrus, has been found to play a critical role in establishing declarative or episodic memory. We measured the neural response in these structures, using event-related functional magnetic resonance imaging, while six healthy subjects performed the retrieval task for facial identity and emotion, respectively. Under the identity condition, the subjects participated in a yes/no recognition test for neutral faces learned before the scanning. Under the emotion condition, the subjects learned the faces with positive or negative expression and retrieved their expressions from neutral cue faces. The results showed that the left hippocampus is primarily involved in the identification of learned faces, and that the adjacent parahippocampal gyrus responds more to target than to distracter events. These results indicate a specific engagement of the left hippocampal regions in conscious recollection and identification of physiognomic facial features. The activity in the right hippocampus increased under both the identity and emotion conditions. The present results may relate with the functional model of face recognition in which the left hemisphere contributes to the processing of detailed features and the right hemisphere is efficient in the processing of global features.     

The visual analysis of emotional actions

This study examined the neural substrates of facial familiarity and person-knowledge. Based on current neural models of face perception, it was hypothesized that distinct extended networks of brain regions differentiate the perception of (a) novel faces, (b) novel faces associated with person-knowledge, (c) perceptually familiar faces and (d) familiar faces for which person-knowledge was learned. To test this hypothesis, we conducted an event-related functional magnetic resonance imaging experiment during which participants viewed faces experimentally manipulated to represent these different levels of familiarity. Results confirmed that distinct networks of brain regions, particularly the medial prefrontal cortex, underlie the perception of faces for which person-knowledge is available.     

Neural substrates for the recognition of newly learned faces: a functional MRI study

Face recognition is critical to the appreciation of our social and physical relations. Functional magnetic resonance imaging (fMRI) was used to identify brain regions involved in the recognition of newly learned faces. Two experiments were conducted. Experiment 1 contrasted a fixation control task with a face recognition task in which subjects were exposed solely to previously viewed faces (all-target). Experiment 2 compared a fixation control with another face recognition task in which subjects were presented with both novel and viewed faces (half-target). Compared to the fixation control, the all-target face recognition was associated with activation in the bilateral occipital and occipitotemporal regions, whereas the half-target face recognition produced activation in the right parietal and prefrontal regions, in addition to the occipital and occipitotemporal. The all-target minus half-target comparison revealed significant activation in the bilateral fusiform gyrus, suggesting stronger fusiform activity during the all-target than the half-target face recognition. The half-target minus all-target comparison showed significant activation in the superior and inferior parietal lobules and several regions in the right frontal lobe. These findings demonstrated that the bilateral fusiform gyrus is involved, not only in face perception, but in a certain aspect of face recognition memory and that this aspect is related to the actual recognition of previously viewed faces rather than the processing of novel ones, which results are consistent with previous lesion work. The right parietal and frontal regions, in contrast, are differentially more associated with the processes related to the detection of novel faces or retrieval effort.     

Face gender modulates women’s brain activity during face encoding

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.     

Memory for friends or foes: The social context of past encounters with faces modulates their subsequent neural traces in the brain

Abstract

Every day we encounter new people, interact with them, and form person impressions based on quick and automatic inferences from minimal contextual information. Previous studies have identified an extensive network of brain areas involved in familiar face recognition, but there is little evidence to date concerning the neural bases of negative vs. positive person impressions. In the present study, participants were repeatedly exposed to 16 unfamiliar face identities within a pseudo-interactive game context to generate a perception of either “friends” or “foes”. Functional magnetic resonance imaging (fMRI) was then performed during an old/new memory task to assess any difference in brain responses to these now familiar face identities, relative to unfamiliar faces. Importantly, whereas facial expressions were always emotional (either smiling or angry) during the encoding phase, they were always neutral during the memory task. Our results reveal that several brain regions involved in familiar face recognition, including fusiform cortex, posterior cingulate gyrus, and amygdala, plus additional areas involved in motivational control such as caudate and anterior cingulate cortex, were differentially modulated as a function of a previous encounter, and generally more activated when faces were perceived as “foes” rather than “friends”. These findings underscore that a key dimension of social judgments, based on past impressions of who may be supportive or hostile, may lead to long-lasting effects on memory for faces and thus influence affective reactions to people during a subsequent encounter even in a different (neutral) context.     

N250 ERP correlates of the acquisition of face representations across different images

We used ERPs to investigate neural correlates of face learning. At learning, participants viewed video clips of unfamiliar people, which were presented either with or without voices providing semantic information. In a subsequent face-recognition task (four trial blocks), learned faces were repeated once per block and presented interspersed with novel faces. To disentangle face from image learning, we used different images for face repetitions. Block effects demonstrated that engaging in the face-recognition task modulated ERPs between 170 and 900 msec poststimulus onset for learned and novel faces. In addition, multiple repetitions of different exemplars of learned faces elicited an increased bilateral N250. Source localizations of this N250 for learned faces suggested activity in fusiform gyrus, similar to that found previously for N250r in repetition priming paradigms [Schweinberger, S. R., Pickering, E. C., Jentzsch, I., Burton, A. M., & Kaufmann, J. M. Event-related brain potential evidence for a response of inferior temporal cortex to familiar face repetitions. Cognitive Brain Research, 14, 398-409, 2002]. Multiple repetitions of learned faces also elicited increased central-parietal positivity between 400 and 600 msec and caused a bilateral increase of inferior-temporal negativity (>300 msec) compared with novel faces. Semantic information at learning enhanced recognition rates. Faces that had been learned with semantic information elicited somewhat less negative amplitudes between 700 and 900 msec over left inferior-temporal sites. Overall, the findings demonstrate a role of the temporal N250 ERP in the acquisition of new face representations across different images. They also suggest that, compared with visual presentation alone, additional semantic information at learning facilitates postperceptual processing in recognition but does not facilitate perceptual analysis of learned faces.     

Neural substrates for recognition of familiar voices: a PET study.

Identification of familiar people is essential in our social life. We can identify familiar people by hearing their voices as well as by viewing their faces. By measuring regional cerebral blood flow (rCBF) by positron emission tomography (PET), we identified neural substrates for the recognition of familiar voices. The brain activity during discrimination of voices of the subjects' associates and friends from those of unfamiliar people was compared with that during an analogous discrimination of their own voice from unfamiliar voices as well as during vowel discrimination. The left frontal pole, right temporal pole, right entorhinal cortex, and left precuneus were activated to a greater extent during discrimination of familiar voice than during control discriminations, suggesting that these brain regions are involved in the recognition of familiar voices. Furthermore, the adjusted values of rCBF in the left frontal pole and right temporal pole correlated with the number of subjects' correct identification of familiar voices. The present results suggest that these two regions are coactively associated with matching the currently heard voice to familiar voices in one's memory.     

Differential neural activity and connectivity for processing one's own face: A preliminary report

The experience of self is unique and pivotal to clinically relevant cognitive and emotional functions. However, well-controlled data on specialized brain regions and functional networks underlying the experience of self remain limited. This functional magnetic resonance imaging study investigated neural activity and connectivity specific to processing one's own face in healthy women by examining neural responses to the pictures of the subjects' own faces in contrast to faces of their own mothers, female friends and strangers during passive viewing, emotional and self-relevance evaluations. The processing of one's own face in comparison to processing of familiar faces revealed significant activity in right anterior insula (AI) and left inferior parietal lobule (IPL), and less activity in right posterior cingulate/precuneus (PCC/PCu) across all tasks. Further, the seed-based correlation analysis of right AI, and left IPL, showed differential functional networks in self and familiar faces contrasts. There were no differences in valence and saliency ratings between self and familiar others. Our preliminary results suggest that the self-experience cued by self-face is processed predominantly by brain regions and related networks that link interoceptive feelings and sense of body ownership to self-awareness and less by regions of higher order functioning such as autobiographical memories.     

Differential neural activity and connectivity for processing one's own face: a preliminary report

The experience of self is unique and pivotal to clinically relevant cognitive and emotional functions. However, well-controlled data on specialized brain regions and functional networks underlying the experience of self remain limited. This functional magnetic resonance imaging study investigated neural activity and connectivity specific to processing one's own face in healthy women by examining neural responses to the pictures of the subjects' own faces in contrast to faces of their own mothers, female friends and strangers during passive viewing, emotional and self-relevance evaluations. The processing of one's own face in comparison to processing of familiar faces revealed significant activity in right anterior insula (AI) and left inferior parietal lobule (IPL), and less activity in right posterior cingulate/precuneus (PCC/PCu) across all tasks. Further, the seed-based correlation analysis of right AI, and left IPL, showed differential functional networks in self and familiar faces contrasts. There were no differences in valence and saliency ratings between self and familiar others. Our preliminary results suggest that the self-experience cued by self-face is processed predominantly by brain regions and related networks that link interoceptive feelings and sense of body ownership to self-awareness and less by regions of higher order functioning such as autobiographical memories.     

Prosopagnosia and object agnosia without covert recognition

Investigations of the visual recognition abilities of the patient M.S. are reported. M.S. is unable to achieve overt recognition of any familiar faces, and many everyday objects. In Task 1 he showed semantic priming from name primes but not from face primes in a name recognition task. In Task 2 he showed no advantage in learning true (face + correct name) rather than untrue (face + someone else's name) pairings of faces and names. In Task 3 semantic priming of lexical decision was only found for object picture primes that M.S. was able to recognize overtly. In Task 4 faster matching of photographs of familiar than unfamiliar objects was only found for objects that M.S. was able to recognize overtly. These findings demonstrate an absence of covert recognition effects for M.S., consistent with the view that his impairment is primarily "perceptual" in nature.     

A fifteen year follow-up of a case of developmental prosopagnosia.

The term developmental prosopagnosia refers to an impairment in the recognition of familiar faces which has been present from birth in the absence of neurological disease or birth complications. The first reported study was by McConachie (1976, Cortex, 12: 76-82) and we report here a fifteen year follow-up on this case (AB). Recently developed theoretical models postulating separate processes involved in face perception and recognition were used to guide the exploration of her functional deficit. Our investigations with AB showed that basic visuo-sensory functions (acuity, contrast sensitivity, colour, etc.) were largely intact. General face perception (e.g. distinguishing between a face and a "nonface") was relatively well preserved. Recognition of familiar faces was severely impaired and she also showed problems with other face processing tasks (e.g. analysis of facial expression) and in object recognition. In object recognition she made errors based on visual similarity, and she had problems identifying exemplars from categories with many visually similar items. In addition, she was very poor at identifying objects or silhouettes from an unusual viewpoint. We conclude that AB has always been poor at constructing an effective internal representation sufficient to permit recognition of items which are visually difficult to discriminate. Therefore, she may not have been able to acquire useable stored representations either, because this deficit has been present since birth. This functional account was supported by subsequent studies which demonstrated a complete absence of covert face recognition.     

Cross-modal interactions between human faces and voices involved in person recognition

Faces and voices are key features of human recognition but the way the brain links them together is still unknown. In this study, we measured brain activity using functional magnetic resonance imaging (fMRI) while participants were recognizing previously learned static faces, voices and voice–static face associations. Using a subtraction method between bimodal and unimodal conditions, we observed that voice–face associations activated both unimodal visual and auditory areas, and specific multimodal regions located in the left angular gyrus and the right hippocampus. Moreover, a functional connectivity analysis confirmed the connectivity of the right hippocampus with the unimodal areas. These findings demonstrate that binding faces and voices rely on a cerebral network sustaining different aspects of integration such as sensory inputs processing, attention and memory.     

Face familiarity feelings, the right temporal lobe and the possible underlying neural mechanisms

A comprehensive review was made of the relationships between right hemisphere and face familiarity feelings, taking separately into account: (a) studies of patients with unilateral lesions of the anterior or the posterior parts of the right and left temporal lobes, who showed a familiar people recognition disorder, (b) studies of right and left brain-damaged patients, presenting an increased familiarity for unknown persons or abnormal familiarity feelings for well known people, (c) results of studies conducted in normal subjects to evaluate the lateralization of face familiarity feelings. In this last section, we separately reviewed: results obtained by means of separate presentation of familiar and unfamiliar faces to the right and left visual fields; lateralization of event-related potentials evoked by familiar vs unfamiliar faces; results of activation studies presenting familiar and unfamiliar faces. Taken together, results of this review have shown that face familiarity feelings are specifically generated by the right hemisphere. Clinical and neurophysiological data suggest that familiarity feelings: (1) are probably due to a lateralized subcortical route, allowing a first, unconscious, global recognition of familiar faces and (2) facilitate the subsequent distinction of known faces (unconsciously detected) from unfamiliar faces. Results of the review have also shown that the right frontal areas play an important role in the production or monitoring of inappropriate familiarity decisions.     

Brain activation on fMRI and verbal memory ability: functional neuroanatomic correlates of CVLT performance.

We have recently reported (Saykin et al., 1999b) selective activation of left medial temporal lobe structures during processing of novel compared to familiar words using functional magnetic resonance imaging (fMRI). The current study describes the relationship between a widely used clinical test of verbal learning, the California Verbal Learning Test (CVLT), and the previously reported fMRI activations. Thirteen right-handed healthy adult participants were studied with whole brain echo-planar fMRI while listening to novel and recently learned (familiar) words intermixed pseudorandomly in an event-related design. These participants were also tested with the CVLT. Scores for CVLT Trial 1 (immediate encoding of novel words) and recognition discriminability (recognition of familiar vs. novel words) were correlated with fMRI signal change during processing of novel versus familiar words using a covariance model implemented in SPM96. For the novel words analysis, voxels in the right anterior hippocampus correlated significantly with Trial 1 (r = .76 at the maxima). For the recognition analysis, a significant cluster of voxels was found in the right dorsolateral prefrontal cortex (r = .88 at the maxima). Our prior results of separable left medial temporal activation to novel and familiar words, together with results of the covariance analyses reported here, suggest that in addition to the left medial temporal lobe (MTL) regions that are engaged during novel and familiar word processing, the right hippocampus and right frontal lobe are also involved, particularly in those participants with better memory ability. This positive relationship between fMRI activation and CVLT performance suggests a role for these right hemisphere regions in successful memory processing of verbal material, perhaps reflecting more efficient encoding and retrieval strategies that facilitate memory.     

Spatially Adjacent Regions in Posterior Cingulate Cortex Represent Familiar Faces at Different Levels of Complexity

Extensive research has shown that perceptual information of faces is processed in a network of hierarchically-organized areas within ventral temporal cortex. For familiar and famous faces, perceptual processing of faces is normally accompanied by extraction of semantic knowledge about the social status of persons. Semantic processing of familiar faces could entail progressive stages of information abstraction. However, the cortical mechanisms supporting multistage processing of familiar faces have not been characterized. Here, using an event-related fMRI experiment, familiar faces from four celebrity groups (actors, singers, politicians, and football players) and unfamiliar faces were presented to the human subjects (both males and females) while they were engaged in a face categorization task. We systematically explored the cortical representations for faces, familiar faces, subcategories of familiar faces, and familiar face identities using whole-brain univariate analysis, searchlight-based multivariate pattern analysis (MVPA), and functional connectivity analysis. Convergent evidence from all these analyses revealed a set of overlapping regions within posterior cingulate cortex (PCC) that contained decodable fMRI responses for representing different levels of semantic knowledge about familiar faces. Our results suggest a multistage pathway in PCC for processing semantic information of faces, analogous to the multistage pathway in ventral temporal cortex for processing perceptual information of faces.SIGNIFICANCE STATEMENT Recognizing familiar faces is an important component of social communications. Previous research has shown that a distributed network of brain areas is involved in processing the semantic information of familiar faces. However, it is not clear how different levels of semantic information are represented in the brain. Here, we evaluated the multivariate response patterns across the entire cortex to discover the areas that contain information for familiar faces, subcategories of familiar faces, and identities of familiar faces. The searchlight maps revealed that different levels of semantic information are represented in topographically adjacent areas within posterior cingulate cortex (PCC). The results suggest that semantic processing of faces is mediated through progressive stages of information abstraction in PCC.     

Familiarity and face emotion recognition in patients with schizophrenia

Objective

To assess the emotion recognition in familiar and unknown faces in a sample of schizophrenic patients and healthy controls.

Methods

Face emotion recognition of 18 outpatients diagnosed with schizophrenia (DSM-IVTR) and 18 healthy volunteers was assessed with two Emotion Recognition Tasks using familiar faces and unknown faces. Each subject was accompanied by 4 familiar people (parents, siblings or friends), which were photographed by expressing the 6 Ekman’s basic emotions. Face emotion recognition in familiar faces was assessed with this ad hoc instrument. In each case, the patient scored (from 1 to 10) the subjective familiarity and affective valence corresponding to each person.

Results

Patients with schizophrenia not only showed a deficit in the recognition of emotions on unknown faces (p = .01), but they also showed an even more pronounced deficit on familiar faces (p = .001). Controls had a similar success rate in the unknown faces task (mean: 18 +/− 2.2) and the familiar face task (mean: 17.4 +/− 3). However, patients had a significantly lower score in the familiar faces task (mean: 13.2 +/− 3.8) than in the unknown faces task (mean: 16 +/− 2.4; p < .05). In both tests, the highest number of errors was with emotions of anger and fear. Subjectively, the patient group showed a lower level of familiarity and emotional valence to their respective relatives (p < .01).

Conclusions

The sense of familiarity may be a factor involved in the face emotion recognition and it may be disturbed in schizophrenia.