Individuals with adverse childhood experiences explore less and underweight reward feedback.

Adverse childhood experiences (ACEs) are extreme stressors that lead to negative psychosocial outcomes in adulthood. Nonhuman animals explore less after exposure to early stress. Therefore, in this preregistered study, we hypothesized that reduced exploration following ACEs would also be evident in human adults. Further, we predicted that adults with ACEs, in a foraging task, would adopt a decision-making policy that relies on the most-recent reward feedback, a rational strategy for unstable environments. We analyzed data from 145 adult participants, 47 with four or more ACEs and 98 with fewer than four ACEs. In the foraging task, participants evaluated the trade-off between exploiting a known patch with diminishing rewards and exploring a novel one with a fresh distribution of rewards. Using computational modeling, we quantified the degree to which participants' decisions weighted recent feedback. As predicted, participants with ACEs explored less. However, contrary to our hypothesis, they underweighted recent feedback. These unexpected findings indicate that early adversity may dampen reward sensitivity. Our results may help to identify cognitive mechanisms that link childhood trauma to the onset of psychopathology.

Caricatured facial movements enhance perception of emotional facial expressions.

Although faces "in the wild" constantly undergo complicated movements, humans adeptly perceive facial identity and expression. Previous studies, focusing mainly on identity, used photographic caricature to show that distinctive form increases perceived dissimilarity. We tested whether distinctive facial movements showed similar effects, and we focussed on both perception of expression and identity. We caricatured the movements of an animated computer head, using physical motion metrics extracted from videos. We verified that these "ground truth" metrics showed the expected effects: Caricature increased physical dissimilarity between faces differing in expression and those differing in identity. Like the ground truth dissimilarity, participants' dissimilarity perception was increased by caricature when faces differed in expression. We found these perceived dissimilarities to reflect the "representational geometry" of the ground truth. However, neither of these findings held for faces differing in identity. These findings replicated across two paradigms: pairwise ratings and multiarrangement. In a final study, motion caricature did not improve recognition memory for identity, whether manipulated at study or test. We report several forms of converging evidence for spatiotemporal caricature effects on dissimilarity perception of different expressions. However, more work needs to be done to discover what identity-specific movements can enhance face identification.

Face space representations of movement.

The challenging computational problem of perceiving dynamic faces "in the wild" goes unresolved because most research focuses on easier questions about static photograph perception. This literature conceptualizes face representation as a dissimilarity-based "face space", with axes that describe the dimensions of static images. Some versions express positions in face space relative to a central tendency (norm). Are facial movements represented like this? We tested for representations that accord with an a priori hypothesized motion-based face space by experimentally manipulating faces' motion-based dissimilarity. Because we caricatured movements, we could test for representations of dissimilarity from a motion-based norm. Behaviorally, participants perceived these caricatured expressions as convincing and recognizable. Moreover, as expected, caricature enhanced perceived dissimilarity between facial expressions. Functional magnetic resonance imaging showed that occipitotemporal brain responses, including face-selective and motion-sensitive areas, reflect this face space. This evidence converged across methods including analysis of univariate mean responses (which additionally exhibited norm-based responses), repetition suppression and representational similarity analysis. This accumulated evidence for "representational geometry" shows how perception and visual brain responses to facial dynamics reflect representations of movement-based dissimilarity spaces, including explicit computation of distance from a norm movement.

Looking for Mr(s) Right: Decision bias can prevent us from finding the most attractive face.

In realistic and challenging decision contexts, people may show biases that prevent them from choosing their favored options. For example, astronomer Johannes Kepler famously interviewed several candidate fiancées sequentially, but was rejected when attempting to return to a previous candidate. Similarly, we examined human performance on searches for attractive faces through fixed-length sequences by adapting optimal stopping computational theory developed from behavioral ecology and economics. Although economics studies have repeatedly found that participants sample too few options before choosing the best-ranked number from a series, we instead found overlong searches with many sequences ending without choice. Participants employed irrationally high choice thresholds, compared to the more lax, realistic standards of a Bayesian ideal observer, which achieved better-ranked faces. We consider several computational accounts and find that participants most resemble a Bayesian model that decides based on altered attractiveness values. These values may produce starkly different biases in the facial attractiveness domain than in other decision domains.

Effective Connectivity from Early Visual Cortex to Posterior Occipitotemporal Face Areas Supports Face Selectivity and Predicts Developmental Prosopagnosia.

Face processing is mediated by interactions between functional areas in the occipital and temporal lobe, and the fusiform face area (FFA) and anterior temporal lobe play key roles in the recognition of facial identity. Individuals with developmental prosopagnosia (DP), a lifelong face recognition impairment, have been shown to have structural and functional neuronal alterations in these areas. The present study investigated how face selectivity is generated in participants with normal face processing, and how functional abnormalities associated with DP, arise as a function of network connectivity. Using functional magnetic resonance imaging and dynamic causal modeling, we examined effective connectivity in normal participants by assessing network models that include early visual cortex (EVC) and face-selective areas and then investigated the integrity of this connectivity in participants with DP. Results showed that a feedforward architecture from EVC to the occipital face area, EVC to FFA, and EVC to posterior superior temporal sulcus (pSTS) best explained how face selectivity arises in both controls and participants with DP. In this architecture, the DP group showed reduced connection strengths on feedforward connections carrying face information from EVC to FFA and EVC to pSTS. These altered network dynamics in DP contribute to the diminished face selectivity in the posterior occipitotemporal areas affected in DP. These findings suggest a novel view on the relevance of feedforward projection from EVC to posterior occipitotemporal face areas in generating cortical face selectivity and differences in face recognition ability. SIGNIFICANCE STATEMENT: Areas of the human brain showing enhanced activation to faces compared to other objects or places have been extensively studied. However, the factors leading to this face selectively have remained mostly unknown. We show that effective connectivity from early visual cortex to posterior occipitotemporal face areas gives rise to face selectivity. Furthermore, people with developmental prosopagnosia, a lifelong face recognition impairment, have reduced face selectivity in the posterior occipitotemporal face areas and left anterior temporal lobe. We show that this reduced face selectivity can be predicted by effective connectivity from early visual cortex to posterior occipitotemporal face areas. This study presents the first network-based account of how face selectivity arises in the human brain.

Low-frequency oscillations employ a general coding of the spatio-temporal similarity of dynamic faces.

Brain networks use neural oscillations as information transfer mechanisms. Although the face perception network in occipitotemporal cortex is well-studied, contributions of oscillations to face representation remain an open question. We tested for links between oscillatory responses that encode facial dimensions and the theoretical proposal that faces are encoded in similarity-based "face spaces". We quantified similarity-based encoding of dynamic faces in magnetoencephalographic sensor-level oscillatory power for identity, expression, physical and perceptual similarity of facial form and motion. Our data show that evoked responses manifest physical and perceptual form similarity that distinguishes facial identities. Low-frequency induced oscillations (< 20Hz) manifested more general similarity structure, which was not limited to identity, and spanned physical and perceived form and motion. A supplementary fMRI-constrained source reconstruction implicated fusiform gyrus and V5 in this similarity-based representation. These findings introduce a potential link between "face space" encoding and oscillatory network communication, which generates new hypotheses about the potential oscillation-mediated mechanisms that might encode facial dimensions.

Facial-Attractiveness Choices Are Predicted by Divisive Normalization.

Do people appear more attractive or less attractive depending on the company they keep? A divisive-normalization account-in which representation of stimulus intensity is normalized (divided) by concurrent stimulus intensities-predicts that choice preferences among options increase with the range of option values. In the first experiment reported here, I manipulated the range of attractiveness of the faces presented on each trial by varying the attractiveness of an undesirable distractor face that was presented simultaneously with two attractive targets, and participants were asked to choose the most attractive face. I used normalization models to predict the context dependence of preferences regarding facial attractiveness. The more unattractive the distractor, the more one of the targets was preferred over the other target, which suggests that divisive normalization (a potential canonical computation in the brain) influences social evaluations. I obtained the same result when I manipulated faces' averageness and participants chose the most average face. This finding suggests that divisive normalization is not restricted to value-based decisions (e.g., attractiveness). This new application to social evaluation of normalization, a classic theory, opens possibilities for predicting social decisions in naturalistic contexts such as advertising or dating.

Network Interactions Explain Sensitivity to Dynamic Faces in the Superior Temporal Sulcus.

The superior temporal sulcus (STS) in the human and monkey is sensitive to the motion of complex forms such as facial and bodily actions. We used functional magnetic resonance imaging (fMRI) to explore network-level explanations for how the form and motion information in dynamic facial expressions might be combined in the human STS. Ventral occipitotemporal areas selective for facial form were localized in occipital and fusiform face areas (OFA and FFA), and motion sensitivity was localized in the more dorsal temporal area V5. We then tested various connectivity models that modeled communication between the ventral form and dorsal motion pathways. We show that facial form information modulated transmission of motion information from V5 to the STS, and that this face-selective modulation likely originated in OFA. This finding shows that form-selective motion sensitivity in the STS can be explained in terms of modulation of gain control on information flow in the motion pathway, and provides a substantial constraint for theories of the perception of faces and biological motion.

Cross-frequency power coupling between hierarchically organized face-selective areas.

Neural oscillations are linked to perception and behavior and may reflect mechanisms for long-range communication between brain areas. We developed a causal model of oscillatory dynamics in the face perception network using magnetoencephalographic data from 51 normal volunteers. This model predicted induced responses to faces by estimating oscillatory power coupling between source locations corresponding to bilateral occipital and fusiform face areas (OFA and FFA) and the right superior temporal sulcus (STS). These sources showed increased alpha and theta and decreased beta power as well as selective responses to fearful facial expressions. We then used Bayesian model comparison to compare hypothetical models, which were motivated by previous connectivity data and a well-known theory of temporal lobe function. We confirmed this theory in detail by showing that the OFA bifurcated into 2 independent, hierarchical, feedforward pathways, with fearful expressions modulating power coupling only in the more dorsal (STS) pathway. The power coupling parameters showed a common pattern over connections. Low-frequency bands showed same-frequency power coupling, which, in the dorsal pathway, was modulated by fearful faces. Also, theta power showed a cross-frequency suppression of beta power. This combination of linear and nonlinear mechanisms could reflect computational mechanisms in hierarchical feedforward networks.

Top-down control of visual responses to fear by the amygdala.

The visual cortex is sensitive to emotional stimuli. This sensitivity is typically assumed to arise when amygdala modulates visual cortex via backwards connections. Using human fMRI, we compared dynamic causal connectivity models of sensitivity with fearful faces. This model comparison tested whether amygdala modulates distinct cortical areas, depending on dynamic or static face presentation. The ventral temporal fusiform face area showed sensitivity to fearful expressions in static faces. However, for dynamic faces, we found fear sensitivity in dorsal motion-sensitive areas within hMT+/V5 and superior temporal sulcus. The model with the greatest evidence included connections modulated by dynamic and static fear from amygdala to dorsal and ventral temporal areas, respectively. According to this functional architecture, amygdala could enhance encoding of fearful expression movements from video and the form of fearful expressions from static images. The amygdala may therefore optimize visual encoding of socially charged and salient information.

Dynamic and static facial expressions decoded from motion-sensitive areas in the macaque monkey.

Humans adeptly use visual motion to recognize socially relevant facial information. The macaque provides a model visual system for studying neural coding of expression movements, as its superior temporal sulcus (STS) possesses brain areas selective for faces and areas sensitive to visual motion. We used functional magnetic resonance imaging and facial stimuli to localize motion-sensitive areas [motion in faces (Mf) areas], which responded more to dynamic faces compared with static faces, and face-selective areas, which responded selectively to faces compared with objects and places. Using multivariate analysis, we found that information about both dynamic and static facial expressions could be robustly decoded from Mf areas. By contrast, face-selective areas exhibited relatively less facial expression information. Classifiers trained with expressions from one motion type (dynamic or static) showed poor generalization to the other motion type, suggesting that Mf areas employ separate and nonconfusable neural codes for dynamic and static presentations of the same expressions. We also show that some of the motion sensitivity elicited by facial stimuli was not specific to faces but could also be elicited by moving dots, particularly in fundus of the superior temporal and middle superior temporal polysensory/lower superior temporal areas, confirming their already well established low-level motion sensitivity. A different pattern was found in anterior STS, which responded more to dynamic than to static faces but was not sensitive to dot motion. Overall, we show that emotional expressions are mostly represented outside of face-selective cortex, in areas sensitive to motion. These regions may play a fundamental role in enhancing recognition of facial expression despite the complex stimulus changes associated with motion.

Understanding patch foraging strategies across development.

Patch foraging is a near-ubiquitous behaviour across the animal kingdom and characterises many decision-making domains encountered by humans. We review how a disposition to explore in adolescence may reflect the evolutionary conditions under which hunter-gatherers foraged for resources. We propose that neurocomputational mechanisms responsible for reward processing, learning, and cognitive control facilitate the transition from exploratory strategies in adolescence to exploitative strategies in adulthood - where individuals capitalise on known resources. This developmental transition may be disrupted by psychopathology, as there is emerging evidence of biases in explore/exploit choices in mental health problems. Explore/exploit choices may be an informative marker for mental health across development and future research should consider this feature of decision-making as a target for clinical intervention.

Hominoid-specific sulcal variability is related to face perception ability.

The relationship among brain structure, brain function, and behavior is of major interest in neuroscience, evolutionary biology, and psychology. This relationship is especially intriguing when considering hominoid-specific brain structures because they cannot be studied in widely examined models in neuroscience such as mice, marmosets, and macaques. The fusiform gyrus (FG) is a hominoid-specific structure critical for face processing that is abnormal in individuals with developmental prosopagnosia (DPs)-individuals who have severe deficits recognizing the faces of familiar people in the absence of brain damage. While previous studies have found anatomical and functional differences in the FG between DPs and NTs, no study has examined the shallow tertiary sulcus (mid-fusiform sulcus, MFS) within the FG that is a microanatomical, macroanatomical, and functional landmark in humans, as well as was recently shown to be present in non-human hominoids. Here, we implemented pre-registered analyses of neuroanatomy and face perception in NTs and DPs. Results show that the MFS was shorter in DPs than NTs. Furthermore, individual differences in MFS length in the right, but not left, hemisphere predicted individual differences in face perception. These results support theories linking brain structure and function to perception, as well as indicate that individual differences in MFS length can predict individual differences in face processing. Finally, these findings add to growing evidence supporting a relationship between morphological variability of late developing, tertiary sulci and individual differences in cognition.

Parietal cortex and insula relate to evidence seeking relevant to reward-related decisions.

Decisions are most effective after collecting sufficient evidence to accurately predict rewarding outcomes. We investigated whether human participants optimally seek evidence and we characterized the brain areas associated with their evidence seeking. Participants viewed sequences of bead colors drawn from hidden urns and attempted to infer the majority bead color in each urn. When viewing each bead color, participants chose either to seek more evidence about the urn by drawing another bead (draw choices) or to infer the urn contents (urn choices). We then compared their evidence seeking against that predicted by a Bayesian ideal observer model. By this standard, participants sampled less evidence than optimal. Also, when faced with urns that had bead color splits closer to chance (60/40 versus 80/20) or potential monetary losses, participants increased their evidence seeking, but they showed less increase than predicted by the ideal observer model. Functional magnetic resonance imaging showed that urn choices evoked larger hemodynamic responses than draw choices in the insula, striatum, anterior cingulate, and parietal cortex. These parietal responses were greater for participants who sought more evidence on average and for participants who increased more their evidence seeking when draws came from 60/40 urns. The parietal cortex and insula were associated with potential monetary loss. Insula responses also showed modulation with estimates of the expected gains of urn choices. Our findings show that participants sought less evidence than predicted by an ideal observer model and their evidence-seeking behavior may relate to responses in the insula and parietal cortex.

Fusiform gyrus face selectivity relates to individual differences in facial recognition ability.

Regions of the occipital and temporal lobes, including a region in the fusiform gyrus (FG), have been proposed to constitute a "core" visual representation system for faces, in part because they show face selectivity and face repetition suppression. But recent fMRI studies of developmental prosopagnosics (DPs) raise questions about whether these measures relate to face processing skills. Although DPs manifest deficient face processing, most studies to date have not shown unequivocal reductions of functional responses in the proposed core regions. We scanned 15 DPs and 15 non-DP control participants with fMRI while employing factor analysis to derive behavioral components related to face identification or other processes. Repetition suppression specific to facial identities in FG or to expression in FG and STS did not show compelling relationships with face identification ability. However, we identified robust relationships between face selectivity and face identification ability in FG across our sample for several convergent measures, including voxel-wise statistical parametric mapping, peak face selectivity in individually defined "fusiform face areas" (FFAs), and anatomical extents (cluster sizes) of those FFAs. None of these measures showed associations with behavioral expression or object recognition ability. As a group, DPs had reduced face-selective responses in bilateral FFA when compared with non-DPs. Individual DPs were also more likely than non-DPs to lack expected face-selective activity in core regions. These findings associate individual differences in face processing ability with selectivity in core face processing regions. This confirms that face selectivity can provide a valid marker for neural mechanisms that contribute to face identification ability.

Neural prediction of higher-order auditory sequence statistics.

During auditory perception, we are required to abstract information from complex temporal sequences such as those in music and speech. Here, we investigated how higher-order statistics modulate the neural responses to sound sequences, hypothesizing that these modulations are associated with higher levels of the peri-Sylvian auditory hierarchy. We devised second-order Markov sequences of pure tones with uniform first-order transition probabilities. Participants learned to discriminate these sequences from random ones. Magnetoencephalography was used to identify evoked fields in which second-order transition probabilities were encoded. We show that improbable tones evoked heightened neural responses after 200 ms post-tone onset during exposure at the learning stage or around 150 ms during the subsequent test stage, originating near the right temporoparietal junction. These signal changes reflected higher-order statistical learning, which can contribute to the perception of natural sounds with hierarchical structures. We propose that our results reflect hierarchical predictive representations, which can contribute to the experiences of speech and music.

Voxel-based morphometry reveals reduced grey matter volume in the temporal cortex of developmental prosopagnosics.

Individuals with developmental prosopagnosia exhibit severe and lasting difficulties in recognizing faces despite the absence of apparent brain abnormalities. We used voxel-based morphometry to investigate whether developmental prosopagnosics show subtle neuroanatomical differences from controls. An analysis based on segmentation of T1-weighted images from 17 developmental prosopagnosics and 18 matched controls revealed that they had reduced grey matter volume in the right anterior inferior temporal lobe and in the superior temporal sulcus/middle temporal gyrus bilaterally. In addition, a voxel-based morphometry analysis based on the segmentation of magnetization transfer parameter maps showed that developmental prosopagnosics also had reduced grey matter volume in the right middle fusiform gyrus and the inferior temporal gyrus. Multiple regression analyses relating three distinct behavioural component scores, derived from a principal component analysis, to grey matter volume revealed an association between a component related to facial identity and grey matter volume in the left superior temporal sulcus/middle temporal gyrus plus the right middle fusiform gyrus/inferior temporal gyrus. Grey matter volume in the lateral occipital cortex was associated with component scores related to object recognition tasks. Our results demonstrate that developmental prosopagnosics have reduced grey matter volume in several regions known to respond selectively to faces and provide new evidence that integrity of these areas relates to face recognition ability.

Maturation of speech and language functional neuroanatomy in pediatric normal controls.

PURPOSE: This study explores the relationship between age and resting-state regional cerebral blood flow (rCBF) in regions associated with higher order language skills using a population of normal children, adolescents, and young adults. METHOD: rCBF was measured in 33 normal participants between the ages of 7 and 19 years using single photon emission computed tomography. Participants' ages were regressed on rCBF values (normalized to whole-brain CBF) in 2 ways: (a) within anatomically defined, language-related regions of interest (ROIs) including Wernicke's area, Broca's area, angular gyrus, planum temporale, and Heschl's gyrus and (b) within clusters of voxels found to be significantly related to age in voxel-wise analyses. RESULTS: rCBF in all anatomically defined ROIs except Heschl's gyrus declined as a function of age. Additionally, voxel-wise analyses revealed clusters where rCBF declined with age in left inferior parietal, left superior temporal, and right middle temporal regions-areas often implicated in higher order language functions. CONCLUSIONS: These data suggest that ongoing maturation (e.g., dendritic pruning) in higher order cognitive areas (e.g., angular gyrus) continues into adolescence, as reflected by declining rCBF, while the primary auditory area (Heschl's gyrus) has become a stable neuronal population by age 7 years.

Structural and effective connectivity reveals potential network-based influences on category-sensitive visual areas.

Visual category perception is thought to depend on brain areas that respond specifically when certain categories are viewed. These category-sensitive areas are often assumed to be "modules" (with some degree of processing autonomy) and to act predominantly on feedforward visual input. This modular view can be complemented by a view that treats brain areas as elements within more complex networks and as influenced by network properties. This network-oriented viewpoint is emerging from studies using either diffusion tensor imaging to map structural connections or effective connectivity analyses to measure how their functional responses influence each other. This literature motivates several hypotheses that predict category-sensitive activity based on network properties. Large, long-range fiber bundles such as inferior fronto-occipital, arcuate and inferior longitudinal fasciculi are associated with behavioral recognition and could play crucial roles in conveying backward influences on visual cortex from anterior temporal and frontal areas. Such backward influences could support top-down functions such as visual search and emotion-based visual modulation. Within visual cortex itself, areas sensitive to different categories appear well-connected (e.g., face areas connect to object- and motion sensitive areas) and their responses can be predicted by backward modulation. Evidence supporting these propositions remains incomplete and underscores the need for better integration of DTI and functional imaging.