Age differences in Neural Activation to Face Trustworthiness: Voxel Pattern and Activation Level Assessments.

Judgment of trustworthiness is an important social ability. Many studies show neural activation differences to variations in face trustworthiness in brain reward regions. A previously published analysis of the present fMRI data showed that older adults' (OA) reward region activation responded significantly to trustworthiness in a set of older and younger faces, whereas younger adults' (YA) activation did not-a finding inconsistent with studies that used only younger faces. We hypothesized that voxel pattern analyses would be more sensitive to YA neural responses to trustworthiness in our set of faces, replicating YA neural discrimination in prior literature. Based on evidence for OA neural dedifferentiation, we also hypothesized that voxel pattern analyses would more accurately classify YA than OA neural responses to face trustworthiness. We reanalyzed the data with two pattern classification models and evaluated the models' performance with permutation testing. Voxel patterns discriminated face trustworthiness levels in both YA and OA reward regions, while allowing better classification of face trustworthiness for YA than OA, the reverse of previous results for neural activation levels. The moderation of age differences by analytic method shines a light on the possibility that voxel patterns uniquely index neural representations of the stimulus information content, consistent with findings of impaired representation with age.

Differential magnocellular versus parvocellular pathway contributions to the combinatorial processing of facial threat.

Recently, speed of presentation of facially expressive stimuli was found to influence the processing of compound threat cues (e.g., anger/fear/gaze). For instance, greater amygdala responses were found to clear (e.g., direct gaze anger/averted gaze fear) versus ambiguous (averted gaze anger/direct gaze fear) combinations of threat cues when rapidly presented (33 and 300ms), but greater to ambiguous versus clear threat cues when presented for more sustained durations (1, 1.5, and 2s). A working hypothesis was put forth (Adams et al., 2012) that these effects were due to differential magnocellular versus parvocellular pathways contributions to the rapid versus sustained processing of threat, respectively. To test this possibility directly here, we restricted visual stream processing in the fMRI environment using facially expressive stimuli specifically designed to bias visual input exclusively to the magnocellular versus parvocellular pathways. We found that for magnocellular-biased stimuli, activations were predominantly greater to clear versus ambiguous threat-gaze pairs (on par with that previously found for rapid presentations of threat cues), whereas activations to ambiguous versus clear threat-gaze pairs were greater for parvocellular-biased stimuli (on par with that previously found for sustained presentations). We couch these findings in an adaptive dual process account of threat perception and highlight implications for other dual process models within psychology.

Line-Drawn Scenes Provide Sufficient Information for Discrimination of Threat and Mere Negativity.

Previous work using color photographic scenes has shown that human observers are keenly sensitive to different types of threatening and negative stimuli and reliably classify them by the presence, and spatial and temporal directions of threat. To test whether such distinctions can be extracted from impoverished visual information, we used 500 line drawings made by hand-tracing the original set of photographic scenes. Sixty participants rated the scenes on spatial and temporal dimensions of threat. Based on these ratings, trend analysis revealed five scene categories that were comparable to those identified for the matching color photographic scenes. Another 61 participants were randomly assigned to rate the valence or arousal evoked by the line drawings. The line drawings perceived to be the most negative were also perceived to be the most arousing, replicating the finding for color photographic scenes. We demonstrate here that humans are very sensitive to the spatial and temporal directions of threat even when they must extract this information from simple line drawings, and rate the line drawings very similarly to matched color photographs. The set of 500 hand-traced line-drawing scenes has been made freely available to the research community: http://www.kveragalab.org/threat.html.

Dietary dopamine depletion blunts reward network sensitivity to face trustworthiness.

Research demonstrating responsiveness of the neural reward network to face trustworthiness has not assessed whether the effects are mediated by dopaminergic function. We filled this gap in the literature by investigating whether dietary dopamine depletion would blunt the sensitivity of neural activation to faces varying in trustworthiness across reward regions as well as the sensitivity of behavioral responses to those faces. As prolactin release is negatively regulated by dopamine, peripheral prolactin levels confirmed the efficacy of our manipulation. The dopamine depletion manipulation moderated neural activation to face trustworthiness in the amygdala, medial orbital frontal cortex, and ventral medial prefrontal cortex. Control participants ( n=20) showed nonlinear and linear neural activation to face trustworthiness in the amygdala and ventral medial prefrontal cortex, and nonlinear activation in the medial orbital frontal cortex, while depleted participants ( n=20) showed only a linear effect in the amygdala. Controls also showed stronger amygdala activation to high trustworthy faces than depleted participants. In contrast to effects on neural activation, dopamine depletion did not blunt the sensitivity of behavioral ratings. While this is the first study to demonstrate that dopamine depletion blunts the sensitivity of the neural reward system to social stimuli, namely faces varying in trustworthiness, future research should investigate behavioral measures that may be more responsive to dopaminergic effects than face ratings. Such research would shed further light on the possibility that individual differences in dopaminergic function that were simulated by our manipulation influence social interactions with people who vary in facial trustworthiness.

Sex-related differences in behavioral and amygdalar responses to compound facial threat cues.

During face perception, we integrate facial expression and eye gaze to take advantage of their shared signals. For example, fear with averted gaze provides a congruent avoidance cue, signaling both threat presence and its location, whereas fear with direct gaze sends an incongruent cue, leaving threat location ambiguous. It has been proposed that the processing of different combinations of threat cues is mediated by dual processing routes: reflexive processing via magnocellular (M) pathway and reflective processing via parvocellular (P) pathway. Because growing evidence has identified a variety of sex differences in emotional perception, here we also investigated how M and P processing of fear and eye gaze might be modulated by observer's sex, focusing on the amygdala, a structure important to threat perception and affective appraisal. We adjusted luminance and color of face stimuli to selectively engage M or P processing and asked observers to identify emotion of the face. Female observers showed more accurate behavioral responses to faces with averted gaze and greater left amygdala reactivity both to fearful and neutral faces. Conversely, males showed greater right amygdala activation only for M-biased averted-gaze fear faces. In addition to functional reactivity differences, females had proportionately greater bilateral amygdala volumes, which positively correlated with behavioral accuracy for M-biased fear. Conversely, in males only the right amygdala volume was positively correlated with accuracy for M-biased fear faces. Our findings suggest that M and P processing of facial threat cues is modulated by functional and structural differences in the amygdalae associated with observer's sex.

Older adults' neural activation in the reward circuit is sensitive to face trustworthiness.

We examined older adult (OA) and younger adult (YA) neural sensitivity to face trustworthiness in reward circuit regions, previously found to respond to trustworthiness in YA. Interactions of face trustworthiness with age revealed effects exclusive to OA in the amygdala and caudate, and an effect that was not moderated by age in the dorsal anterior cingulate cortex (dACC). OA, but not YA, showed a nonlinear amygdala response to face trustworthiness, with significantly stronger activation response to high than to medium trustworthy faces, and no difference between low and medium or high. This may explain why an earlier study investigating OA amygdala activation to trustworthiness failed to find a significant effect, since only the linear low versus high trustworthiness difference was assessed. OA, but not YA, also showed significantly stronger activation to high than to low trustworthy faces in the right caudate, indicating a positive linear effect, consistent with previous YA research, as well as significantly stronger activation to high than to medium but not low trustworthy faces in the left caudate, indicating a nonlinear effect. Activation in dACC across both age groups showed a positive linear effect consistent with previous YA research. Finally, OA rated the faces as more trustworthy than did YA across all levels of trustworthiness. Future research should examine whether the null effects for YA were due to our inclusion of older faces. Research also should investigate possible implications of our findings for more ecologically valid OA responses to people who vary in facial trustworthiness.

Observer's anxiety facilitates magnocellular processing of clear facial threat cues, but impairs parvocellular processing of ambiguous facial threat cues.

Facial expression and eye gaze provide a shared signal about threats. While a fear expression with averted gaze clearly points to the source of threat, direct-gaze fear renders the source of threat ambiguous. Separable routes have been proposed to mediate these processes, with preferential attunement of the magnocellular (M) pathway to clear threat, and of the parvocellular (P) pathway to threat ambiguity. Here we investigated how observers' trait anxiety modulates M- and P-pathway processing of clear and ambiguous threat cues. We scanned subjects (N = 108) widely ranging in trait anxiety while they viewed fearful or neutral faces with averted or directed gaze, with the luminance and color of face stimuli calibrated to selectively engage M- or P-pathways. Higher anxiety facilitated processing of clear threat projected to M-pathway, but impaired perception of ambiguous threat projected to P-pathway. Increased right amygdala reactivity was associated with higher anxiety for M-biased averted-gaze fear, while increased left amygdala reactivity was associated with higher anxiety for P-biased, direct-gaze fear. This lateralization was more pronounced with higher anxiety. Our findings suggest that trait anxiety differentially affects perception of clear (averted-gaze fear) and ambiguous (direct-gaze fear) facial threat cues via selective engagement of M and P pathways and lateralized amygdala reactivity.

The Older Adult Positivity Effect in Evaluations of Trustworthiness: Emotion Regulation or Cognitive Capacity?

An older adult positivity effect, i.e., the tendency for older adults to favor positive over negative stimulus information more than do younger adults, has been previously shown in attention, memory, and evaluations. This effect has been attributed to greater emotion regulation in older adults. In the case of attention and memory, this explanation has been supported by some evidence that the older adult positivity effect is most pronounced for negative stimuli, which would motivate emotion regulation, and that it is reduced by cognitive load, which would impede emotion regulation. We investigated whether greater older adult positivity in the case of evaluative responses to faces is also enhanced for negative stimuli and attenuated by cognitive load, as an emotion regulation explanation would predict. In two studies, younger and older adults rated trustworthiness of faces that varied in valence both under low and high cognitive load, with the latter manipulated by a distracting backwards counting task. In Study 1, face valence was manipulated by attractiveness (low /disfigured faces, medium, high/fashion models' faces). In Study 2, face valence was manipulated by trustworthiness (low, medium, high). Both studies revealed a significant older adult positivity effect. However, contrary to an emotion regulation account, this effect was not stronger for more negative faces, and cognitive load increased rather than decreased the rated trustworthiness of negatively valenced faces. Although inconsistent with emotion regulation, the latter effect is consistent with theory and research arguing that more cognitive resources are required to process negative stimuli, because they are more cognitively elaborated than positive ones. The finding that increased age and increased cognitive load both enhanced the positivity of trustworthy ratings suggests that the older adult positivity effect in evaluative ratings of faces may reflect age-related declines in cognitive capacity rather than increases in the regulation of negative emotions.

Dedifferentiated face processing in older adults is linked to lower resting state metabolic activity in fusiform face area.

We used multimodal brain imaging to examine possible mediators of age-related neural dedifferentiation (less specific neural activation) to different categories of stimuli that had been shown in previous research. Specifically, we examined resting blood flow and brain activation in areas involved in object, place and face perception. We observed lower activation, specificity, and resting blood flow for older adults (OA) than younger adults (YA) in the fusiform face area (FFA) but not in the other regions of interest. Mediation analyses further revealed that FFA resting state blood flow mediated age differences in FFA specificity, whereas age differences in visual and cognitive function and cortical thickness did not. Whole brain analyses also revealed more activated voxels for all categories in OA, as well as more frontal activation for faces but not for the other categories in OA than YA. Less FFA specificity coupled with more frontal activation when passively viewing faces suggest that OA have more difficulty recruiting specialized face processing mechanisms, and the lower FFA metabolic activity even when faces are not being processed suggests an OA deficiency in the neural substrate underlying face processing. Our data point to a detuning of face-selective mechanisms in older adults.

Face Shape and Behavior: Implications of Similarities in Infants and Adults.

We investigated conceptual overlap between literature demonstrating links between adult facial width-to-height ratio (FWHR) and behavior and that demonstrating links between infant FWHR and temperament by investigating whether babyfaceness is associated with FWHR and behavior at both ages. Babyfaceness was positively correlated with FWHR in both infants and adults. Babyfaceness also was correlated with an infant temperament that is a precursor of bolder behavior in childhood and adulthood, just as a broader infant FWHR was previously shown to be. These results call into question existing explanations for relationships between facial appearance and adult assertive or aggressive behavior. Previously, behavioral correlates of adult FWHR have been attributed to influences of pubertal testosterone, and correlates of adult babyfaceness have been attributed to compensation for undesirable stereotypes. Our findings indicate that the pre-natal developmental influences required to explain appearance-temperament relationships in infancy also should be considered as explanations for appearance-behavior relationships in adulthood.

If it bleeds, it leads: separating threat from mere negativity.

Most theories of emotion hold that negative stimuli are threatening and aversive. Yet in everyday experiences some negative sights (e.g. car wrecks) attract curiosity, whereas others repel (e.g. a weapon pointed in our face). To examine the diversity in negative stimuli, we employed four classes of visual images (Direct Threat, Indirect Threat, Merely Negative and Neutral) in a set of behavioral and functional magnetic resonance imaging studies. Participants reliably discriminated between the images, evaluating Direct Threat stimuli most quickly, and Merely Negative images most slowly. Threat images evoked greater and earlier blood oxygen level-dependent (BOLD) activations in the amygdala and periaqueductal gray, structures implicated in representing and responding to the motivational salience of stimuli. Conversely, the Merely Negative images evoked larger BOLD signal in the parahippocampal, retrosplenial, and medial prefrontal cortices, regions which have been implicated in contextual association processing. Ventrolateral as well as medial and lateral orbitofrontal cortices were activated by both threatening and Merely Negative images. In conclusion, negative visual stimuli can repel or attract scrutiny depending on their current threat potential, which is assessed by dynamic shifts in large-scale brain network activity.

Older and younger adults' accuracy in discerning health and competence in older and younger faces.

We examined older and younger adults' accuracy judging the health and competence of faces. Accuracy differed significantly from chance and varied with face age but not rater age. Health ratings were more accurate for older than younger faces, with the reverse for competence ratings. Accuracy was greater for low attractive younger faces, but not for low attractive older faces. Greater accuracy judging older faces' health was paralleled by greater validity of attractiveness and looking older as predictors of their health. Greater accuracy judging younger faces' competence was paralleled by greater validity of attractiveness and a positive expression as predictors of their competence. Although the ability to recognize variations in health and cognitive ability is preserved in older adulthood, the effects of face age on accuracy and the different effects of attractiveness across face age may alter social interactions across the life span.

Age similarities in recognizing threat from faces and diagnostic cues.

BACKGROUND: Previous research indicates that younger adults (YA) can identify men's tendency to be aggressive based merely on their neutral expression faces. We compared older adults (OA) and YA accuracy and investigated contributing facial cues. METHOD: In Study 1, YA and OA rated the aggressiveness of young men depicted in facial photographs in a control, distraction, or accuracy motivation condition. In Study 2, YA and OA rated how angry, attractive, masculine, and babyfaced the men looked in addition to rating their aggressiveness. These measures plus measured facial width-to-height ratio (FWHR) were used to examine cues to aggressiveness. RESULTS: Accuracy coefficients, calculated by correlating rated aggressiveness with the men's previously measured actual aggressiveness, were significant and equal for OA and YA. Accuracy was not moderated by distraction or accuracy motivation, suggesting automatic processing. A greater FWHR, lower attractiveness, and higher masculinity independently influenced rated aggressiveness by both age groups and also were valid cues to actual aggressiveness. DISCUSSION: Despite previous evidence for positivity biases in OA, they can be just as accurate as YA when it comes to discerning actual differences in the aggressiveness of young men.

Perception of social cues of danger in autism spectrum disorders.

Intuitive grasping of the meaning of subtle social cues is particularly affected in autism spectrum disorders (ASD). Despite their relevance in social communication, the effect of averted gaze in fearful faces in conveying a signal of environmental threat has not been investigated using real face stimuli in adults with ASD. Here, using functional MRI, we show that briefly presented fearful faces with averted gaze, previously shown to be a strong communicative signal of environmental danger, produce different patterns of brain activation than fearful faces with direct gaze in a group of 26 normally intelligent adults with ASD compared with 26 matched controls. While implicit cue of threat produces brain activation in attention, emotion processing and mental state attribution networks in controls, this effect is absent in individuals with ASD. Instead, individuals with ASD show activation in the subcortical face-processing system in response to direct eye contact. An effect of differences in looking behavior was excluded in a separate eye tracking experiment. Our data suggest that individuals with ASD are more sensitive to direct eye contact than to social signals of danger conveyed by averted fearful gaze.

The missing link: enhanced functional connectivity between amygdala and visceroceptive cortex in migraine.

BACKGROUND: Migraine is a neurovascular disorder in which altered functional connectivity between pain-modulating circuits and the limbic system may play a role. Cortical spreading depression (CSD), which underlies migraine aura (MWA), induces C-fos expression in the amygdala. The role of CSD and amygdala connectivity in migraine without aura (MwoA) is less clear and may differentiate migraine from other chronic pain disorders. METHODS: Using resting-state functional MRI, we compared functional connectivity between the amygdala and the cortex in MWA and MWoA patients as well as in healthy subjects and in two other chronic pain conditions not associated with CSD: trigeminal neuralgia (TGN) and carpal tunnel syndrome (CTS). RESULTS: Amygdala connectivity in both MWA and MWoA was increased to the visceroceptive insula relative to all other groups examined. CONCLUSION: The observed increased connectivity within the limbic/viscerosensory network, present only in migraineurs, adds to the evidence of a neurolimbic pain network dysfunction and may reflect repetitive episodes of CSD leading to the development of migraine pain.

Altered functional magnetic resonance imaging resting-state connectivity in periaqueductal gray networks in migraine.

OBJECTIVE: The periaqueductal gray matter (PAG), a known modulator of somatic pain transmission, shows evidence of interictal functional and structural abnormalities in migraineurs, which may contribute to hyperexcitability along spinal and trigeminal nociceptive pathways, and lead to the migraine attack. The aim of this study was to examine functional connectivity of the PAG in migraine. METHODS: Using resting-state functional MRI, we compared functional connectivity between PAG and a subset of brain areas involved in nociceptive/somatosensory processing and pain modulation in 17 subjects with migraine, during a pain-free state, versus 17 gender- and age-matched controls. We also assessed the relation between intrinsic resting-state correlations within PAG networks and the average monthly frequency of migraine attacks, as well as allodynia. RESULTS: Our findings show stronger connectivity between the PAG and several brain areas within nociceptive and somatosensory processing pathways in migraineurs versus controls. In addition, as the monthly frequency of migraine attacks worsens, the strength of the connectivity in some areas within these pathways increases, whereas a significant decrease in functional resting-state connectivity between the PAG and brain regions with a predominant role in pain modulation (prefrontal cortex, anterior cingulate, amygdala) can be evidenced. Finally, migraineurs with a history of allodynia exhibit significantly reduced connectivity between PAG, prefrontal regions, and anterior cingulate compared to migraineurs without allodynia. INTERPRETATION: These data reveal interictal dysfunctional dynamics within pain pathways in migraine manifested as an impairment of the descending pain modulatory circuits, likely leading to loss of pain inhibition, and hyperexcitability primarily in nociceptive areas.

Magnocellular projections as the trigger of top-down facilitation in recognition.

Object recognition is traditionally viewed as a hierarchical, bottom-up neural process. This view has been challenged recently by theoretical models and by findings indicating that top-down processes are involved in facilitating recognition. However, how such high-level information can be activated quickly enough to facilitate the bottom-up processing is yet unknown. We propose that such top-down facilitation is triggered by magnocellular information projected early and rapidly to the orbitofrontal cortex. Using human neuroimaging, we show that stimuli designed to bias processing toward the magnocellular pathway differentially activated the orbitofrontal cortex compared with parvocellular-biased stimuli. Although the magnocellular stimuli had a lower contrast than the parvocellular stimuli, they were recognized faster and just as accurately. Moreover, orbitofrontal activity predicted the performance advantage for the magnocellular, but not for the parvocellular-biased, stimuli, whereas the opposite was true in the fusiform gyrus. Last, analyses of effective connectivity using dynamic causal modeling showed that magnocellular-biased stimuli significantly activated pathways from occipital visual cortex to orbitofrontal cortex and from orbitofrontal cortex to fusiform gyrus. Conversely, parvocellular-biased stimuli significantly activated a pathway from the occipital visual cortex to fusiform gyrus. Our findings support the proposal that fast magnocellular projections linking early visual and inferotemporal object recognition regions with the orbitofrontal cortex facilitate object recognition by enabling the generation of early predictions.