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1.  Changes in “Top-Down” Connectivity Underlie Repetition Suppression in the Ventral Visual Pathway 
Repetition of the same stimulus leads to a reduction in neural activity known as repetition suppression (RS). In functional magnetic resonance imaging (fMRI), RS is found for multiple object categories. One proposal is that RS reflects locally based “within-region” changes, such as neural fatigue. Thus, if a given region shows RS across changes in stimulus size or view, then it is inferred to hold size- or view-invariant representations. An alternative hypothesis characterizes RS as a consequence of “top-down” between-region modulation. Differentiating between these accounts is central to the correct interpretation of fMRI RS data. It is also unknown whether the same mechanisms underlie RS to identical stimuli and RS across changes in stimulus size or view. Using fMRI, we investigated RS within a body-sensitive network in human visual cortex comprising the extrastriate body area (EBA) and the fusiform body area (FBA). Both regions showed RS to identical images of the same body that was unaffected by changes in body size or view. Dynamic causal modeling demonstrated that changes in backward, top-down (FBA-to-EBA) effective connectivity play a critical role in RS. Furthermore, only repetition of the identical image showed additional changes in forward connectivity (EBA-to-FBA). These results suggest that RS is driven by changes in top-down modulation, whereas the contribution of “feedforward” changes in connectivity is dependent on the precise nature of the repetition. Our results challenge previous interpretations regarding the underlying nature of neural representations made using fMRI RS paradigms.
doi:10.1523/JNEUROSCI.5013-10.2011
PMCID: PMC3759805  PMID: 21490204
2.  Eye gaze is not coded by cardinal mechanisms alone 
Gaze is an important social cue in regulating human and non-human interactions. In this study, we employed an adaptation paradigm to examine the mechanisms underlying the perception of another's gaze. Previous research has shown that the interleaved presentation of leftwards and rightwards gazing adaptor stimuli results in observers judging a wider range of gaze deviations as being direct. We applied a similar paradigm to examine how human observers encode oblique (e.g. upwards and to the left) directions of gaze. We presented observers with interleaved gaze adaptors and examined whether adaptation differed between congruent (adaptor and test along same axis) and incongruent conditions. We find greater adaptation in congruent conditions along cardinal (horizontal and vertical) and non-cardinal (oblique) directions suggesting gaze is not coded alone by cardinal mechanisms. Our results suggest that the functional aspects of gaze processing might parallel that of basic visual features such as orientation.
doi:10.1098/rspb.2013.1049
PMCID: PMC3712425  PMID: 23782886
gaze; adaptation; cardinal; non-cardinal
3.  Reduced gaze aftereffects are related to difficulties categorising gaze direction in children with autism 
Neuropsychologia  2013;51(8):1504-1509.
Perceptual mechanisms are generally flexible or “adaptive”, as evidenced by perceptual aftereffects: distortions that arise following exposure to a stimulus. We examined whether adaptive mechanisms for coding gaze direction are atypical in children diagnosed with an autism spectrum condition. Twenty-four typical children and 24 children with autism, of similar age and ability, were administered a developmentally sensitive eye-gaze adaptation task. In the pre-adaptation phase, children judged whether target faces showing subtle deviations in eye-gaze direction were looking leftwards, rightwards or straight-ahead. Next, children were adapted to faces gazing in one consistent direction (25° leftwards/rightwards) before categorising the direction of the target faces again. Children with autism showed difficulties in judging whether subtle deviations in gaze were directed to the left, right or straight-ahead relative to typical children. Although adaptation to leftward or rightward gaze resulted in reduced sensitivity to gaze on the adapted side for both groups, the aftereffect was significantly reduced in children with autism. Furthermore, the magnitude of children's gaze aftereffects was positively related to their ability to categorise gaze direction. These results show that the mechanisms coding gaze are less flexible in autism and offer a potential new explanation for these children's difficulties discriminating subtle deviations in gaze direction.
Highlights
•Adaptive mechanisms are fundamental for perceptual coding.•We found adaptation to gaze direction was significantly attenuated in autism.•The degree of adaptation was also linked to children's gaze acuity.•This study provides potential evidence for the functional benefits of adaptation.
doi:10.1016/j.neuropsychologia.2013.03.021
PMCID: PMC3708125  PMID: 23583965
Autism; Gaze; Adaptation; Aftereffect; Vision
4.  Humans Have an Expectation That Gaze Is Directed Toward Them 
Current Biology  2013;23(8):717-721.
Summary
Many animals use cues from another animal’s gaze to help distinguish friend from foe [1–3]. In humans, the direction of someone’s gaze provides insight into their focus of interest and state of mind [4] and there is increasing evidence linking abnormal gaze behaviors to clinical conditions such as schizophrenia and autism [5–11]. This fundamental role of another’s gaze is buoyed by the discovery of specific brain areas dedicated to encoding directions of gaze in faces [12–14]. Surprisingly, however, very little is known about how others’ direction of gaze is interpreted. Here we apply a Bayesian framework that has been successfully applied to sensory and motor domains [15–19] to show that humans have a prior expectation that other people’s gaze is directed toward them. This expectation dominates perception when there is high uncertainty, such as at night or when the other person is wearing sunglasses. We presented participants with synthetic faces viewed under high and low levels of uncertainty and manipulated the faces by adding noise to the eyes. Then, we asked the participants to judge relative gaze directions. We found that all participants systematically perceived the noisy gaze as being directed more toward them. This suggests that the adult nervous system internally represents a prior for gaze and highlights the importance of experience in developing our interpretation of another’s gaze.
Highlights
► A novel application of a Bayesian framework to gaze perception ► We tend to perceive others’ gaze as directed toward us when not certain ► Head orientation influences perceived eye direction, even when only the eye region is visible
doi:10.1016/j.cub.2013.03.030
PMCID: PMC3918857  PMID: 23562265
5.  Failure to deactivate the default mode network indicates a possible endophenotype of autism 
Molecular Autism  2012;3:15.
Background
Reduced activity during cognitively demanding tasks has been reported in the default mode network in typically developing controls and individuals with autism. However, no study has investigated the default mode network (DMN) in first-degree relatives of those with autism (such as siblings) and it is not known whether atypical activation of the DMN is specific to autism or whether it is also present in unaffected relatives. Here we use functional magnetic resonance imaging to investigate the pattern of task-related deactivation during completion of a visual search task, the Embedded Figures Task, in teenagers with autism, their unaffected siblings and typically developing controls.
Findings
We identified striking reductions in deactivation during the Embedded Figures Task in unaffected siblings compared to controls in brain regions corresponding to the default mode network. Adolescents with autism and their unaffected siblings similarly failed to deactivate regions, including posterior cingulate and bilateral inferior parietal cortex.
Conclusions
This suggests that a failure to deactivate these regions is a functional endophenotype of autism, related to familial risk for the condition shared between individuals with autism and their siblings.
doi:10.1186/2040-2392-3-15
PMCID: PMC3539860  PMID: 23206727
Autism; Default mode network; Functional MRI; Endophenotype
6.  5-HTTLPR–environment interplay and its effects on neural reactivity in adolescents 
Neuroimage  2012;63-248(3):1670-1680.
It is not known how 5-HTTLPR genotype × childhood adversity (CA) interactions that are associated with an increased risk for affective disorders in population studies operate at the neural systems level. We hypothesized that healthy adolescents at increased genetic and environmental risk for developing mood disorders (depression and anxiety) would demonstrate increased amygdala reactivity to emotional stimuli compared to those with only one such risk factor or those with none. Participants (n = 67) were classified into one of 4 groups dependent on being homozygous for the long or short alleles within the serotonin-transporter-linked polymorphic region (5-HTTLPR) of the SLC6A4 gene and exposure to CA in the first 11 years of life (present or absent). A functional magnetic resonance imaging investigation was undertaken which involved viewing emotionally-salient face stimuli. In addition, we assessed the role of other variables hypothesized to influence amygdala reactivity, namely recent negative life-events (RNLE) assessed at ages 14 and 17, current anxiety symptoms and psychiatric history. We replicated prior findings demonstrating moderation by gene variants in 5-HTTLPR, but found no support for an effect of CA on amygdala reactivity. We also found a significant effect of RNLE aged 17 with amygdala reactivity demonstrating additive, but not interactive effects with 5-HTTLPR. A whole-brain analysis found a 5-HTTLPR × CA interaction in the lingual gyrus whereby CA appears to differentially modify neural reactivity depending on genotype. These results demonstrate that two different forms of environmental adversities interplay with 5-HTTLPR and thereby differentially impact amygdala and cortical reactivity.
Highlights
► Tested hypothesis that amygdala is neural locus for 5-HTTLPR × environment interaction ► Additive effects of 5-HTTLPR genotype and recent life events on amygdala reactivity ► Genotype × childhood adversity interaction on neural reactivity in lingual gyrus ► Two forms of environmental adversities interplay with 5-HTTLPR and neural reactivity. ► No support for hypothesized G × E interaction on amygdala reactivity
doi:10.1016/j.neuroimage.2012.07.067
PMCID: PMC3480648  PMID: 23034517
5-HTTLPR, (serotonin-transporter-linked polymorphic region); SLC6A4, (Solute carrier family 6 (neurotransmitter transporter, serotonin), member 4); CA, (Childhood adversity); PH, (Psychiatric history); RNLE, (Recent negative life events); CAMEEI, (Cambridge Early Experience Interview); fMRI, (functional magnetic resonance imaging); MFQ, (Mood and Feelings Questionnaire); SAI, (Spielberger Anxiety Inventory); K-SADS-PL, (Kiddie Schedule for Affective Disorders and Schizophrenia for School-Age Children—Present and Lifetime version; 5-HTTLPR; Childhood adversity; Recent negative life events; Amygdala; Functional magnetic resonance imaging; Faces
7.  Facial Expressions of Threat Influence Perceived Gaze Direction in 8 Year-Olds 
PLoS ONE  2012;7(11):e49317.
Adults show reciprocal influences between the perception of gaze direction and emotional expression. These facilitate the understanding of facial signals, because the meaning of one cue can vary considerably depending on the value of the other. Here we ask whether children show similar reciprocal influences in the perception of gaze and expression. A previous study has demonstrated that gaze direction affects the perception of emotional expression in children. Here we demonstrate the opposite direction of influence, showing that expression affects the perception of gaze direction. Specifically, we show that the cone of gaze, i.e., range of gaze deviations perceived as direct, is larger for angry than neutral or fearful faces in 8 year-old children. Therefore, we conclude that children, like adults, show reciprocal influences in the perception of gaze and expression. An unexpected finding was that, compared with adults, children showed larger effects of expression on gaze perception. This finding raises the possibility that it is the ability to process cues independently, rather than sensitivity to combinations, that matures during development. Alternatively, children may be particularly sensitive to anger in adult faces.
doi:10.1371/journal.pone.0049317
PMCID: PMC3498150  PMID: 23166638
8.  Atypical activation during the Embedded Figures Task as a functional magnetic resonance imaging endophenotype of autism 
Brain  2012;135(11):3469-3480.
Atypical activation during the Embedded Figures Task has been demonstrated in autism, but has not been investigated in siblings or related to measures of clinical severity. We identified atypical activation during the Embedded Figures Task in participants with autism and unaffected siblings compared with control subjects in a number of temporal and frontal brain regions. Autism and sibling groups, however, did not differ in terms of activation during this task. This suggests that the pattern of atypical activation identified may represent a functional endophenotype of autism, related to familial risk for the condition shared between individuals with autism and their siblings. We also found that reduced activation in autism relative to control subjects in regions including associative visual and face processing areas was strongly correlated with the clinical severity of impairments in reciprocal social interaction. Behavioural performance was intact in autism and sibling groups. Results are discussed in terms of atypical information processing styles or of increased activation in temporal and frontal regions in autism and the broader phenotype. By separating the aspects of atypical activation as markers of familial risk for the condition from those that are autism-specific, our findings offer new insight into the factors that might cause the expression of autism in families, affecting some children but not others.
doi:10.1093/brain/aws229
PMCID: PMC3501969  PMID: 23065480
autism; Embedded Figures Task; siblings; functional MRI; endophenotype
9.  The amygdala response to images with impact 
Effective photojournalism provokes an emotional reaction and leaves a lasting impression upon the viewer. Striking and memorable images are often said to possess ’impact’. Within cognitive neuroscience memorable emotional images evoke a greater amygdala response. Research to date has focused on arousal as a causative factor, while the contribution of appraisal dimensions relating to salience of an item, goal relevance, or impact are yet to be addressed. We explored how differences in ratings of impact influenced amygdala activity to negative emotional images matched for valence, arousal and other factors. Increased amygdala activation was found to high impact when compared to neutral images, or high impact when compared to low impact images (matched for arousal). Our findings demonstrate that the amygdala response to emotional stimuli is not a function of arousal (or valence) alone and accord more with the proposal that the amygdala responds to the significance or relevance of an event.
doi:10.1093/scan/nsn048
PMCID: PMC2686226  PMID: 19151376
Emotion; Arousal; Attention; Appraisal; fMRI
10.  The Interaction Between Gaze and Facial Expression in the Amygdala and Extended Amygdala is Modulated by Anxiety 
Behavioral evidence indicates that angry faces are seen as more threatening, and elicit greater anxiety, when directed at the observer, whereas the influence of gaze on the processing of fearful faces is less consistent. Recent research has also found inconsistent effects of expression and gaze direction on the amygdala response to facial signals of threat. However, such studies have failed to consider the important influence of anxiety on the response to signals of threat; an influence that is well established in behavioral research and recent neuroimaging studies. Here, we investigated the way in which individual differences in anxiety would influence the interactive effect of gaze and expression on the response to angry and fearful faces in the human extended amygdala. Participants viewed images of fearful, angry and neutral faces, either displaying an averted or direct gaze. We found that state anxiety predicted an increased response in the dorsal amygdala/substantia innominata (SI) to angry faces when gazing at, relative to away from the observer. By contrast, high state anxious individuals showed an increased amygdala response to fearful faces that was less dependent on gaze. In addition, the relationship between state anxiety and gaze on emotional intensity ratings mirrored the relationship between anxiety and the amygdala/SI response. These results have implications for understanding the functional role of the amygdala and extended amygdala in processing signals of threat, and are consistent with the proposed role of this region in coding the relevance or significance of a stimulus to the observer.
doi:10.3389/fnhum.2010.00056
PMCID: PMC2906373  PMID: 20661452
emotion; anxiety; fMRI; face processing; amygdala; expression; gaze
11.  Anxiety and Sensitivity to Gaze Direction in Emotionally Expressive Faces 
Emotion (Washington, D.C.)  2007;7(3):478-486.
This study investigated the role of neutral, happy, fearful, and angry facial expressions in enhancing orienting to the direction of eye gaze. Photographs of faces with either direct or averted gaze were presented. A target letter (T or L) appeared unpredictably to the left or the right of the face, either 300 ms or 700 ms after gaze direction changed. Response times were faster in congruent conditions (i.e., when the eyes gazed toward the target) relative to incongruent conditions (when the eyes gazed away from the target letter). Facial expression did influence reaction times, but these effects were qualified by individual differences in self-reported anxiety. High trait-anxious participants showed an enhanced orienting to the eye gaze of faces with fearful expressions relative to all other expressions. In contrast, when the eyes stared straight ahead, trait anxiety was associated with slower responding when the facial expressions depicted anger. Thus, in anxiety-prone people attention is more likely to be held by an expression of anger, whereas attention is guided more potently by fearful facial expressions.
doi:10.1037/1528-3542.7.3.478
PMCID: PMC2757723  PMID: 17683204
emotion; facial expression; gaze direction; anxiety; attentional orienting
12.  Reduced functional connectivity within and between ‘social’ resting state networks in autism spectrum conditions 
Individuals with Autism Spectrum Conditions (ASC) have difficulties in social interaction and communication, which is reflected in hypoactivation of brain regions engaged in social processing, such as medial prefrontal cortex (mPFC), amygdala and insula. Resting state studies in ASC have identified reduced connectivity of the default mode network (DMN), which includes mPFC, suggesting that other resting state networks incorporating ‘social’ brain regions may also be abnormal. Using Seed-based Connectivity and Group Independent Component Analysis (ICA) approaches, we looked at resting functional connectivity in ASC between specific ‘social’ brain regions, as well as within and between whole networks incorporating these regions. We found reduced functional connectivity within the DMN in individuals with ASC, using both ICA and seed-based approaches. Two further networks identified by ICA, the salience network, incorporating the insula and a medial temporal lobe network, incorporating the amygdala, showed reduced inter-network connectivity. This was underlined by reduced seed-based connectivity between the insula and amygdala. The results demonstrate significantly reduced functional connectivity within and between resting state networks incorporating ‘social’ brain regions. This reduced connectivity may result in difficulties in communication and integration of information across these networks, which could contribute to the impaired processing of social signals in ASC.
doi:10.1093/scan/nss053
PMCID: PMC3739917  PMID: 22563003
autism; resting state; fMRI
13.  Social cognitive deficits and their neural correlates in progressive supranuclear palsy 
Brain  2012;135(7):2089-2102.
Although progressive supranuclear palsy is defined by its akinetic rigidity, vertical supranuclear gaze palsy and falls, cognitive impairments are an important determinant of patients’ and carers’ quality of life. Here, we investigate whether there is a broad deficit of modality-independent social cognition in progressive supranuclear palsy and explore the neural correlates for these. We recruited 23 patients with progressive supranuclear palsy (using clinical diagnostic criteria, nine with subsequent pathological confirmation) and 22 age- and education-matched controls. Participants performed an auditory (voice) emotion recognition test, and a visual and auditory theory of mind test. Twenty-two patients and 20 controls underwent structural magnetic resonance imaging to analyse neural correlates of social cognition deficits using voxel-based morphometry. Patients were impaired on the voice emotion recognition and theory of mind tests but not auditory and visual control conditions. Grey matter atrophy in patients correlated with both voice emotion recognition and theory of mind deficits in the right inferior frontal gyrus, a region associated with prosodic auditory emotion recognition. Theory of mind deficits also correlated with atrophy of the anterior rostral medial frontal cortex, a region associated with theory of mind in health. We conclude that patients with progressive supranuclear palsy have a multimodal deficit in social cognition. This deficit is due, in part, to progressive atrophy in a network of frontal cortical regions linked to the integration of socially relevant stimuli and interpretation of their social meaning. This impairment of social cognition is important to consider for those managing and caring for patients with progressive supranuclear palsy.
doi:10.1093/brain/aws128
PMCID: PMC3381722  PMID: 22637582
progressive supranuclear palsy; voxel-based morphometry; social cognition; theory of mind; emotion perception
14.  Different Neural Mechanisms within Occipitotemporal Cortex Underlie Repetition Suppression across Same and Different-Size Faces 
Cerebral Cortex (New York, NY)  2012;23(5):1073-1084.
Repetition suppression (RS) (or functional magnetic resonance imaging adaptation) refers to the reduction in blood oxygen level–dependent signal following repeated presentation of a stimulus. RS is frequently used to investigate the role of face-selective regions in human visual cortex and is commonly thought to be a “localized” effect, reflecting fatigue of a neuronal population representing a given stimulus. In contrast, predictive coding theories characterize RS as a consequence of “top-down” changes in between-region modulation. Differentiating between these accounts is crucial for the correct interpretation of RS effects in the face-processing network. Here, dynamic causal modeling revealed that different mechanisms underlie different forms of RS to faces in occipitotemporal cortex. For both familiar and unfamiliar faces, repetition of identical face images (same size) was associated with changes in “forward” connectivity between the occipital face area (OFA) and the fusiform face area (FFA) (OFA-to-FFA). In contrast, RS across image size was characterized by altered “backward” connectivity (FFA-to-OFA). In addition, evidence was higher for models in which information projected directly into both OFA and FFA, challenging the role of OFA as the input stage of the face-processing network. These findings suggest “size-invariant” RS to faces is a consequence of interactions between regions rather than being a localized effect.
doi:10.1093/cercor/bhs070
PMCID: PMC3615345  PMID: 22510534
adaptation; DCM; face-processing; fMRI; predictive-coding
15.  Autism spectrum traits predict the neural response to eye gaze in typical individuals 
Neuroimage  2012;59(4-4):3356-3363.
Autism Spectrum Disorders (ASD) are neurodevelopmental disorders characterised by impaired social interaction and communication, restricted interests and repetitive behaviours. The severity of these characteristics are posited to lie on a continuum extending into the typical population, and typical adults' performance on behavioural tasks that are impaired in ASD is correlated with the extent to which they display autistic traits (as measured by Autism Spectrum Quotient, AQ). Individuals with ASD also show structural and functional differences in brain regions involved in social perception. Here we show that variation in AQ in typically developing individuals is associated with altered brain activity in the neural circuit for social attention perception while viewing others' eye gaze. In an fMRI experiment, participants viewed faces looking at variable or constant directions. In control conditions, only the eye region was presented or the heads were shown with eyes closed but oriented at variable or constant directions. The response to faces with variable vs. constant eye gaze direction was associated with AQ scores in a number of regions (posterior superior temporal sulcus, intraparietal sulcus, temporoparietal junction, amygdala, and MT/V5) of the brain network for social attention perception. No such effect was observed for heads with eyes closed or when only the eyes were presented. The results demonstrate a relationship between neurophysiology and autism spectrum traits in the typical (non-ASD) population and suggest that changes in the functioning of the neural circuit for social attention perception is associated with an extended autism spectrum in the typical population.
Highlights
► Autistic spectrum might extend to typically developing (TD) individuals. ► We studied TD individuals with varying Autism Spectrum Quotient (AQ). ► AQ correlated with BOLD response to viewing variable vs. constant eye gaze. ► AQ did not correlate with response to directional control stimuli. ► Neurophysiology and autism spectrum traits are associated in non-AS individuals.
doi:10.1016/j.neuroimage.2011.10.075
PMCID: PMC3315678  PMID: 22062191
Eye gaze; fMRI; Autism spectrum; Attention; Face perception
16.  Effects of Acute Tryptophan Depletion on Prefrontal-Amygdala Connectivity While Viewing Facial Signals of Aggression 
Biological Psychiatry  2012;71(1):36-43.
Background
Reduced levels of serotonin (5-HT) within prefrontal cortex (PFC)–amygdala circuits have long been implicated in impulsive aggression. However, whether lowering 5-HT alters the dynamic interplay between the PFC and the amygdala has not been directly tested in humans. It is known that manipulating 5-HT via acute tryptophan depletion (ATD) causes variable effects on brain responses to a variety of emotional stimuli, but it remains unclear whether ATD affects functional connectivity in neural networks involved in processing social signals of aggression (e.g., angry faces).
Methods
Thirty healthy individuals were enrolled in a randomized, double-blind, placebo-controlled ATD study. On each treatment, brain responses to angry, sad, and neutral faces were measured with functional magnetic resonance imaging. Two methods (psycho-physiological-interaction in a general linear model and dynamic causal modeling) were used to assess the impact of ATD on the functional connectivity between PFC and amygdala.
Results
Data from 19 subjects were available for the final analyses. A whole-brain psycho-physiological-interaction in a general linear model showed that ATD significantly modulated the connectivity between the amygdala and two PFC regions (ventral anterior cingulate cortex and ventrolateral PFC) when processing angry vs. neutral and angry vs. sad but not sad vs. neutral faces. Dynamic causal modeling corroborated and extended these findings by showing that 5-HT depletion reduced the influence of processing angry vs. neutral faces on circuits within PFC and on PFC–amygdala pathways.
Conclusions
We provide strong support for neurobiological accounts positing that 5-HT significantly influences PFC–amygdala circuits implicated in aggression and other affective behaviors.
doi:10.1016/j.biopsych.2011.07.033
PMCID: PMC3368260  PMID: 21920502
5-HT; amygdala; anterior cingulate cortex; effective connectivity; fMRI; violence
17.  Disgust Enhances the Recollection of Negative Emotional Images 
PLoS ONE  2011;6(11):e26571.
Memory is typically better for emotional relative to neutral images, an effect generally considered to be mediated by arousal. However, this explanation cannot explain the full pattern of findings in the literature. Two experiments are reported that investigate the differential effects of categorical affective states upon emotional memory and the contributions of stimulus dimensions other than pleasantness and arousal to any memory advantage. In Experiment 1, disgusting images were better remembered than equally unpleasant frightening ones, despite the disgusting images being less arousing. In Experiment 2, regression analyses identified affective impact – a factor shown previously to influence the allocation of visual attention and amygdala response to negative emotional images – as the strongest predictor of remembering. These findings raise significant issues that the arousal account of emotional memory cannot readily address. The term impact refers to an undifferentiated emotional response to a stimulus, without requiring detailed consideration of specific dimensions of image content. We argue that ratings of impact relate to how the self is affected. The present data call for further consideration of the theoretical specifications of the mechanisms that lead to enhanced memory for emotional stimuli and their neural substrates.
doi:10.1371/journal.pone.0026571
PMCID: PMC3217922  PMID: 22110588
18.  A Head View-Invariant Representation of Gaze Direction in Anterior Superior Temporal Sulcus 
Current Biology  2011;21(21-2):1817-1821.
Summary
Humans show a remarkable ability to discriminate others' gaze direction, even though a given direction can be conveyed by many physically dissimilar configurations of different eye positions and head views. For example, eye contact can be signaled by a rightward glance in a left-turned head or by direct gaze in a front-facing head. Such acute gaze discrimination implies considerable perceptual invariance. Previous human research found that superior temporal sulcus (STS) responds preferentially to gaze shifts [1], but the underlying representation that supports such general responsiveness remains poorly understood. Using multivariate pattern analysis (MVPA) of human functional magnetic resonance imaging (fMRI) data, we tested whether STS contains a higher-order, head view-invariant code for gaze direction. The results revealed a finely graded gaze direction code in right anterior STS that was invariant to head view and physical image features. Further analyses revealed similar gaze effects in left anterior STS and precuneus. Our results suggest that anterior STS codes the direction of another's attention regardless of how this information is conveyed and demonstrate how high-level face areas carry out fine-grained, perceptually relevant discrimination through invariance to other face features.
Highlights
► Response patterns in superior temporal sulcus (STS) code perceived gaze direction ► Gaze codes are invariant to head view and physical image features in anterior STS ► However, such socially irrelevant features do influence gaze codes in posterior STS ► Anterior STS represents where others attend, regardless of how this is conveyed
doi:10.1016/j.cub.2011.09.025
PMCID: PMC3267037  PMID: 22036180
19.  Direction-Sensitive Codes for Observed Head Turns in Human Superior Temporal Sulcus 
Cerebral Cortex (New York, NY)  2011;22(4):735-744.
Humans and other primates are adept at using the direction of another's gaze or head turn to infer where that individual is attending. Research in macaque neurophysiology suggests that anterior superior temporal sulcus (STS) contains a direction-sensitive code for such social attention cues. By contrast, most human functional Magnetic resonance imaging (fMRI) studies report that posterior STS is responsive to social attention cues. It is unclear whether this functional discrepancy is caused by a species difference or by experimental design differences. Furthermore, social attention cues are dynamic in naturalistic social interaction, but most studies to date have been restricted to static displays. In order to address these issues, we used multivariate pattern analysis of fMRI data to test whether response patterns in human right STS distinguish between leftward and rightward dynamic head turns. Such head turn discrimination was observed in right anterior STS/superior temporal gyrus (STG). Response patterns in this region were also significantly more discriminable for head turn direction than for rotation direction in physically matched ellipsoid control stimuli. Our findings suggest a role for right anterior STS/STG in coding the direction of motion in dynamic social attention cues.
doi:10.1093/cercor/bhr061
PMCID: PMC3306570  PMID: 21709175
face perception; fMRI; gaze; head; MVPA
20.  Personality influences the neural responses to viewing facial expressions of emotion 
Cognitive research has long been aware of the relationship between individual differences in personality and performance on behavioural tasks. However, within the field of cognitive neuroscience, the way in which such differences manifest at a neural level has received relatively little attention. We review recent research addressing the relationship between personality traits and the neural response to viewing facial signals of emotion. In one section, we discuss work demonstrating the relationship between anxiety and the amygdala response to facial signals of threat. A second section considers research showing that individual differences in reward drive (behavioural activation system), a trait linked to aggression, influence the neural responsivity and connectivity between brain regions implicated in aggression when viewing facial signals of anger. Finally, we address recent criticisms of the correlational approach to fMRI analyses and conclude that when used appropriately, analyses examining the relationship between personality and brain activity provide a useful tool for understanding the neural basis of facial expression processing and emotion processing in general.
doi:10.1098/rstb.2010.0362
PMCID: PMC3130379  PMID: 21536554
facial expressions; personality; fMRI; amygdala; anxiety; aggression
21.  Impaired holistic coding of facial expression and facial identity in congenital prosopagnosia 
Neuropsychologia  2011;49(5):1226-1235.
Research highlights
► Congenital prosopagnosics show weak holistic coding of expression and identity. ► Normal expression recognition can result from compensatory strategies. ► There may be a common stage of holistic coding for expression and identity. ► Holistic coding of identity is functionally involved in face identification ability.
We test 12 individuals with congenital prosopagnosia (CP), who replicate a common pattern of showing severe difficulty in recognising facial identity in conjunction with normal recognition of facial expressions (both basic and ‘social’). Strength of holistic processing was examined using standard expression composite and identity composite tasks. Compared to age- and sex-matched controls, group analyses demonstrated that CPs showed weaker holistic processing, for both expression and identity information. Implications are (a) normal expression recognition in CP can derive from compensatory strategies (e.g., over-reliance on non-holistic cues to expression); (b) the split between processing of expression and identity information may take place after a common stage of holistic processing; and (c) contrary to a recent claim, holistic processing of identity is functionally involved in face identification ability.
doi:10.1016/j.neuropsychologia.2011.02.021
PMCID: PMC3083514  PMID: 21333662
Face perception; Identity; Expression; Emotion; Holistic processing; Prosopagnosia
22.  The serotonin transporter gene polymorphism and the effect of baseline on amygdala response to emotional faces 
Neuropsychologia  2011;49(4):674-680.
Research highlights
▶ 5-HTTLPR short allele carriers have greater amygdala response to emotional stimuli. ▶ Increased amygdala activity in s-carriers is consistent regardless of baseline. ▶ The results support a largely phasic model of 5-HTTLPR-mediated amygdala modulation.
Previous research has found that a common polymorphism in the serotonin transporter gene (5-HTTLPR) is an important mediator of individual differences in brain responses associated with emotional behaviour. In particular, relative to individuals homozygous for the l-allele, carriers of the s-allele display heightened amygdala activation to emotional compared to non-emotional stimuli. However, there is some debate as to whether this difference is driven by increased activation to emotional stimuli, resting baseline differences between the groups, or decreased activation to neutral stimuli. We performed functional imaging during an implicit facial expression processing task in which participants viewed angry, sad and neutral faces. In addition to neutral faces, we included two further baseline conditions, houses and fixation. We found increased amygdala activation in s-allele carriers relative to l-homozygotes in response to angry faces compared to neutral faces, houses and fixation. When comparing neutral faces to houses or fixation, we found no significant difference in amygdala response between the two groups. In addition, there was no significant difference between the groups in response to fixation when compared with a houses baseline. Overall, these results suggest that the increased amygdala response observed in s-allele carriers to emotional faces is primarily driven by an increased response to emotional faces rather than a decreased response to neutral faces or an increased resting baseline. The results are discussed in relation to the tonic and phasic hypotheses of 5-HTTLPR-mediated modulation of amygdala activity.
doi:10.1016/j.neuropsychologia.2010.12.013
PMCID: PMC3209561  PMID: 21167188
Serotonin; Amygdala; Facial expressions; fMRI
23.  Leaving a bad taste in your mouth but not in my insula 
Previous research has implicated regions of anterior insula/frontal operculum in processing conspecific facial expressions of disgust. It has been suggested however that there are a variety of disgust facial expression components which relate to the disgust-eliciting stimulus. The nose wrinkle is predominantly associated with irritating or offensive smells, the mouth gape and tongue extrusion with distaste and oral irritation, while a broader range of disgust elicitors including aversive interpersonal contacts and certain moral offenses are associated primarily with the upper lip curl. Using functional magnetic resonance imaging, we show that activity in the anterior insula/frontal operculum is seen only in response to canonical disgust faces, exhibiting the nose wrinkle and upper lip curl, and not in response to distaste facial expressions, exhibiting a mouth gape and tongue protrusion. Canonical disgust expressions also result in activity in brain regions linked to social cognition more broadly, including dorsal medial prefrontal cortex, posterior cingulate cortex, temporo-parietal junction and superior temporal sulcus. We interpret these differences in relation to the relative functional and communicative roles of the different disgust expressions and suggest a significant role for appraisal processes in the insula activation to facial expressions of disgust.
doi:10.1093/scan/nsp018
PMCID: PMC2799946  PMID: 19505971
disgust; fMRI; emotion; insula; distaste
24.  Recognition memory for pictorial material in subclinical depression 
Acta Psychologica  2010;135(3):293-301.
Depression has been associated with impaired recollection of episodic details in tests of recognition memory that use verbal material. In two experiments, the remember/know procedure was employed to investigate the effects of dysphoric mood on recognition memory for pictorial materials that may not be subject to the same processing limitations found for verbal materials in depression. In Experiment 1, where the recognition test took place two weeks after encoding, subclinically depressed participants reported fewer know judgements which were likely to be at least partly due to a remember-to-know shift. Although pictures were accompanied by negative or neutral captions at encoding, no effect of captions on recognition memory was observed. In Experiment 2, where the recognition test occurred soon after viewing the pictures, subclinically depressed participants reported fewer remember judgements. All participants reported more remember judgements for pictures of emotionally negative content than pictures of neutral content. Together, these findings demonstrate that recognition memory for pictorial stimuli is compromised in dysphoric individuals in a way that is consistent with a recollection deficit for episodic detail and also reminiscent of that previously reported for verbal materials. These findings contribute to our developing understanding of how mood and memory interact.
doi:10.1016/j.actpsy.2010.07.015
PMCID: PMC2994638  PMID: 20728865
Depression; Memory; Emotion; Recollection; Familiarity
25.  Facial Expression Recognition, Fear Conditioning, and Startle Modulation in Female Subjects with Conduct Disorder 
Biological Psychiatry  2010;68(3):272-279.
Background
Recent behavioral and psychophysiological studies have provided converging evidence for emotional dysfunction in conduct disorder (CD). Most of these studies focused on male subjects and little is known about emotional processing in female subjects with CD. Our primary aim was to characterize explicit and implicit aspects of emotion function to determine whether deficits in these processes are present in girls with CD.
Methods
Female adolescents with CD (n = 25) and control subjects with no history of severe antisocial behavior and no current psychiatric disorder (n = 30) completed tasks measuring facial expression and facial identity recognition, differential autonomic conditioning, and affective modulation of the startle reflex by picture valence.
Results
Compared with control subjects, participants with CD showed impaired recognition of anger and disgust but no differences in facial identity recognition. Impaired sadness recognition was observed in CD participants high in psychopathic traits relative to those lower in psychopathic traits. Participants with CD displayed reduced skin conductance responses to an aversive unconditioned stimulus and impaired autonomic discrimination between the conditioned stimuli, indicating impaired fear conditioning. Participants with CD also showed reduced startle magnitudes across picture valence types, but there were no significant group differences in the pattern of affective modulation.
Conclusions
Adolescent female subjects with CD exhibited deficits in explicit and implicit tests of emotion function and reduced autonomic responsiveness across different output systems. There were, however, no differences in emotional reactivity. These findings suggest that emotional recognition and learning are impaired in female subjects with CD, consistent with results previously obtained in male subjects with CD.
doi:10.1016/j.biopsych.2010.02.019
PMCID: PMC2954286  PMID: 20447616
Conduct disorder; emotion; face recognition; female; psychopathy

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