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.     

The right hemisphere and the dark side of consciousness

Self-awareness and Theory of Mind comprise the main elements of higher-order consciousness. In attempting to localize these abilities, it appears that regions of the right hemisphere including fronto-temporal regions are capable of sustaining a sense of self-awareness. The right hemisphere appears dominant for tasks involving Theory of Mind as well as deception, which may be important for understanding the brain and laterality in terms of evolution. These findings are critical for our understanding of hemispheric differences in terms of higher-order consciousness.     

Fear Recognition and the Neural Basis of Social Cognition

Recent developments in cognitive neuroscience and neurobiology emphasise the interface between our emotions, our feelings and our ability to interact appropriately in social situations. The neural basis of social cognition is subject to intensive research in both humans and non-human primates, research that is providing exciting, provocative and yet consistent findings. Centre stage is the role of efferent and afferent connectivity between the amygdala and neocortical brain regions, now believed to be critical for the processing of social information. Recent research suggests that a sub-cortical neural pathway, routed through the amygdala, may turn out to be a key player in the mystery of why humans are so prone to disorders of social cognition. This pathway responds to direct eye contact, one of many classes of potential threat. In humans, arousal evoked by this exquisitely social stimulus is modulated and controlled by a variety of specific cortical regions. Neural circuits that evolved for the purpose of fear detection in other's faces, an essentially threatening stimulus, are now associated with the acquisition of social skills and appropriate responsiveness in social encounters.     

Approach or avoidance: Neural correlates of intelligence evaluation from faces

Intelligence is among the key determinants of power and social status in modern societies. In this functional magnetic resonance imaging study, we examined the neural correlates of intelligence evaluation from faces. Participants underwent scans while they evaluated the perceived intelligence and friendliness of faces. We found that medial orbitofrontal cortex activity increased linearly with friendliness ratings. The relationship between perceived intelligence and brain activity was positively linear in the right caudate nucleus and U‐shaped (i.e., strong responses to unintelligent‐looking or intelligent‐looking faces) in the right anterior insula/inferior frontal gyrus. Perceived intelligence was also significantly positively correlated with both friendliness and attractiveness. Furthermore, intelligence rating scores had a positive linear effect on reaction times in the friendliness rating task, suggesting that participants had greater conflicts when making friendliness judgments for faces that appeared to belong to intelligent individuals. In addition, the degree of this effect predicted individual differences in the positive linear modulatory effect of intelligence scores in the right caudate nucleus. Our interpretation was that the activity in the caudate nucleus revealed an approach‐avoidance conflict with regard to highly intelligent people, that is, they were perceived as attractive but also potentially threatening. Although our interpretations are merely suggestive because we did not measure the approach‐avoidance behaviors directly, our findings have important implications for understanding the dynamics of human interaction in modern societies that increasingly allocate power and status based on intelligence.     

Neurons in the amygdala of the monkey with responses selective for faces

To investigate the functions of the amygdala in visual information processing and in emotional and social responses, recordings were made from single neurons in the amygdala of the monkey. A population of neurons (40 of more than 1000 recorded in 4 monkeys) was investigated which responded primarily to faces. These neurons typically (1) responded to some human or monkey faces, which were presented to the monkey through a large aperture shutter so that response latencies could be measured, or were simply shown to the monkey, (2) responded to 2-dimensional representations of these faces, as well as to real 3-dimensional faces, (3) had no responses or only small (less than half maximum) responses to gratings, simple geometrical, other complex 3-D stimuli, or to arousing and aversive stimuli, (4) had response latencies of 110-200 ms, (5) were located in the basal accessory nucleus of the amygdala, (6) responded differently to different faces, as shown by measures of d', and could thus over a population of such neurons code information useful for making different responses to different individuals, (7) could in some cases (9/11 tested) respond to parts of faces, and (8) in a few cases (4/19 tested) responded more to a face which produced an emotional response. A comparison made in three monkeys of the responses of these neurons with the responses of 77 neurons with face-selective responses recorded in the cortex of the superior temporal sulcus (STS) showed that the amygdaloid neurons had longer response latencies (110-200 compared to 90-140 ms), and were in some respects more selective in their responses to different faces. It is suggested that the deficits in social and emotional behavior produced by amygdala lesions could be due in part to damage to a neuronal system specialized in utilizing information from faces so that appropriate social and emotional responses can be made to different individuals.     

Neural correlates of anosognosia for cognitive impairment in Alzheimer's disease

We explored the neural substrate of anosognosia for cognitive impairment in Alzheimer's disease (AD). Two hundred nine patients with mild to moderate dementia and their caregivers assessed patients' cognitive impairment by answering a structured questionnaire. Subjects rated 13 cognitive domains as not impaired or associated with mild, moderate, severe, or very severe difficulties, and a sum score was calculated. Two measures of anosognosia were derived. A patient's self assessment, unconfounded by objective measurements of cognitive deficits such as dementia severity and episodic memory impairment, provided an estimate of impaired self-evaluative judgment about cognition in AD. Impaired self-evaluation was related to a decrease in brain metabolism measured with 18F-2-fluoro-2-deoxy-D-glucose positron emission tomography (FDG-PET) in orbital prefrontal cortex and in medial temporal structures. In a cognitive model of anosognosia, medial temporal dysfunction might impair a comparison mechanism between current information on cognition and personal knowledge. Hypoactivity in orbitofrontal cortex may not allow AD patients to update the qualitative judgment associated with their impaired cognitive abilities. Caregivers perceived greater cognitive impairments than patients did. The discrepancy score between caregiver's and patient's evaluations, an other measure of anosognosia, was negatively related to metabolic activity located in the temporoparietal junction, consistent with an impairment of self-referential processes and perspective taking in AD.     

Dissociable roles of the human somatosensory and superior temporal cortices for processing social face signals

Faces are multi-dimensional stimuli bearing important social signals, such as gaze direction and emotion expression. To test whether perception of these two facial attributes recruits distinct cortical areas within the right hemisphere, we used single-pulse transcranial magnetic stimulation (TMS) in healthy volunteers while they performed two different tasks on the same face stimuli. In each task, two successive faces were presented with varying eye-gaze directions and emotional expressions, separated by a short interval of random duration. TMS was applied over either the right somatosensory cortex or the right superior lateral temporal cortex, 100 or 200 ms after presentation of the second face stimulus. Participants performed a speeded matching task on the second face during one of two possible conditions, requiring judgements about either gaze direction or emotion expression (same/different as the first face). Our results reveal a significant task-stimulation site interaction, indicating a selective TMS-related interference following stimulations of somatosensory cortex during the emotional expression task. Conversely, TMS of the superior lateral temporal cortex selectively interfered with the gaze direction task. We also found that the interference effect was specific to the stimulus content in each condition, affecting judgements of gaze shifts (not static eye positions) with TMS over the right superior temporal cortex, and judgements of fearful expressions (not happy expressions) with TMS over the right somatosensory cortex. These results provide for the first time a double dissociation in normal subjects during social face recognition, due to transient disruption of non-overlapping brain regions. The present study supports a critical role of the somatosensory and superior lateral temporal regions in the perception of fear expression and gaze shift in seen faces, respectively.     

Assessment of a six-week computer-based remediation program for social cognition in chronic schizophrenia

Background

Programs to remediate cognitive deficits have shown promising results in schizophrenia, but remediation of social cognition deficits is less well understood. Social cognitive deficits may cause more disability than the widely recognized neurocognitive deficits, suggesting that this is an area worthy of further investigation.

Aim

Implement and evaluate a brief computerized cognitive remediation program designed to improve memory, attention, and facial affect recognition (FAR) in outpatients with chronic schizophrenia.

Methods

Baseline assessments of FAR and of clinical, cognitive, and psychosocial functioning were completed on 20 males with schizophrenia enrolled in an outpatient rehabilitation program at the Shanghai Mental Health Center (the intervention group) and on 20 males with schizophrenia recruited from among regular outpatients at the Center (the control group). Both groups received treatment as usual, but the intervention group also completed an average of 12.7 sessions of a computer-based remediation program for neurocognitive, social, and FAR functioning over a 6-week period. The baseline measures were repeated in both groups at the end of the 6-week trial.

Results

There were no statistically significant differences in the changes in clinical symptoms (assessed by the Positive and Negative Syndrome Scale, PANSS) or cognitive measures (assessed using the Hong Kong List Learning Test and the Letter-Number Sequencing Task) between the intervention and control groups over the 6-week trial, but there were modest improvements on the PANSS for the intervention group between baseline and after the intervention. There was a significantly greater improvement in the social functioning measure (the Personal and Social Performance scale, PSP) in the intervention group than in the control group. The pre-post change in the total facial recognition score in the intervention group was statistically significant (paired t-test=-2.60, p=0.018), and there was a statistical trend of a greater improvement in facial recognition in the intervention group than in the control group (F_(1,37)=2.93; p=0.092).

Conclusion

Integration of FAR training with a short, computer-administrated cognitive remediation program may improve recognition of facial emotions by individuals with schizophrenia, and, thus, improve their social functioning. But more work on developing the FAR training modules and on testing them in larger, more diverse samples will be needed before this can be recommended as a standard part of cognitive remediation programs.     

Neural systems for social cognition in Klinefelter syndrome (47,XXY): evidence from fMRI

Klinefelter syndrome (KS) is a chromosomal condition (47, XXY) that may help us to unravel gene-brain behavior pathways to psychopathology. The phenotype includes social cognitive impairments and increased risk for autism traits. We used functional MRI to study neural mechanisms underlying social information processing. Eighteen nonclinical controls and thirteen men with XXY were scanned during judgments of faces with regard to trustworthiness and age. While judging faces as untrustworthy in comparison to trustworthy, men with XXY displayed less activation than controls in (i) the amygdala, which plays a key role in screening information for socio-emotional significance, (ii) the insula, which plays a role in subjective emotional experience, as well as (iii) the fusiform gyrus and (iv) the superior temporal sulcus, which are both involved in the perceptual processing of faces and which were also less involved during age judgments in men with XXY. This is the first study showing that KS can be associated with reduced involvement of the neural network subserving social cognition. Studying KS may increase our understanding of the genetic and hormonal basis of neural dysfunctions contributing to abnormalities in social cognition and behavior, which are considered core abnormalities in psychiatric disorders such as autism and schizophrenia.     

Atypical resting synchrony in autism spectrum disorder

Autism spectrum disorder (ASD) is increasingly understood to be associated with aberrant functional brain connectivity. Few studies, however, have described such atypical neural synchrony among specific brain regions. Here, we used magnetoencephalography (MEG) to characterize alterations in functional connectivity in adolescents with ASD through source space analysis of phase synchrony. Resting‐state MEG data were collected from 16 adolescents with ASD and 15 age‐ and sex‐matched typically developing (TD) adolescents. Atlas‐guided reconstruction of neural activity at various cortical and subcortical regions was performed and inter‐regional phase synchrony was calculated in physiologically relevant frequency bands. Using a multilevel approach, we characterized atypical resting‐state synchrony within specific anatomically defined networks as well as altered network topologies at both regional and whole‐network scales. Adolescents with ASD demonstrated frequency‐dependent alterations in inter‐regional functional connectivity. Hyperconnectivity was observed among the frontal, temporal, and subcortical regions in beta and gamma frequency ranges. In contrast, parietal and occipital regions were hypoconnected to widespread brain regions in theta and alpha bands in ASD. Furthermore, we isolated a hyperconnected network in the gamma band in adolescents with ASD which encompassed orbitofrontal, subcortical, and temporal regions implicated in social cognition. Results from graph analyses confirmed that frequency‐dependent alterations of network topologies exist at both global and local levels. We present the first source‐space investigation of oscillatory phase synchrony in resting‐state MEG in ASD. This work provides evidence of atypical connectivity at physiologically relevant time scales and indicates that alterations of functional connectivity in adolescents with ASD are frequency dependent and region dependent. Hum Brain Mapp 35:6049–6066, 2014. © 2014 Wiley Periodicals, Inc.     

Neural processing of social interaction: Coordinate‐based meta‐analytic evidence from human neuroimaging studies

While the action observation and mentalizing networks are considered to play complementary roles in understanding others' goals and intentions, they might be concurrently engaged when processing social interactions. We assessed this hypothesis via three activation‐likelihood‐estimation meta‐analyses of neuroimaging studies on the neural processing of: (a) social interactions, (b) individual actions by the action observation network, and (c) mental states by the mentalizing network. Conjunction analyses and direct comparisons unveiled overlapping and specific regions among the resulting maps. We report quantitative meta‐analytic evidence for a “social interaction network” including key nodes of the action observation and mentalizing networks. An action–social interaction‐mentalizing gradient of activity along the posterior temporal cortex highlighted a hierarchical processing of interactions, from visuomotor analyses decoding individual and shared intentions to in‐depth inferences on actors' intentional states. The medial prefrontal cortex, possibly in conjunction with the amygdala, might provide additional information concerning the affective valence of the interaction. This evidence suggests that the functional architecture underlying the neural processing of interactions involves the joint involvement of the action observation and mentalizing networks. These data might inform the design of rehabilitative treatments for social cognition disorders in pathological conditions, and the assessment of their outcome in randomized controlled trials.