The Privileged Status of Peer Faces: Subordinate-level Neural Representations of Faces in Emerging Adults.

Faces can be represented at a variety of different subordinate levels (e.g., race) that can become "privileged" for visual recognition in perceivers and is reflected as patterns of biases (e.g., own-race bias). The mechanisms encoding privileged status are likely varied, making it difficult to predict how neural systems represent subordinate-level biases in face processing. Here, we investigate the neural basis of subordinate-level representations of human faces in the ventral visual pathway, by leveraging recent behavioral findings indicating the privileged nature of peer faces in identity recognition for adolescents and emerging adults (i.e., ages 18-25 years). We tested 166 emerging adults in a face recognition paradigm and a subset of 31 of these participants in two fMRI task paradigms. We showed that emerging adults exhibit a peer bias in face recognition behavior, which indicates a privileged status for a subordinate-level category of faces that is not predicted based on experience alone. This privileged status of peer faces is supported by multiple neural mechanisms within the ventral visual pathway, including enhanced neural magnitude and neural size in the neural size in the fusiform area (FFA1), which is a critical part of the face-processing network that fundamentally supports the representations of subordinate-level categories of faces. These findings demonstrate organizational principles that the human ventral visual pathway uses to privilege relevant social information in face representations, which is essential for navigating human social interactions. It will be important to understand whether similar mechanisms support representations of other subordinate-level categories like race and gender.

Introducing the female Cambridge face memory test - long form (F-CFMT+).

The Cambridge Face Memory Test (CFMT) is one of the most used assessments of face recognition abilities in the science of face processing. The original task, using White male faces, has been empirically evaluated for psychometric properties (Duchaine & Nakayama, 2006), while the longer and more difficult version (CFMT+; Russell et al., 2009) has not. Critically, no version exists using female faces. Here, we present the Female Cambridge Face Memory Test - Long Form (F-CFMT+) and evaluate the psychometric properties of this task in comparison to the Male Cambridge Face Memory Test - Long Form (M-CFMT+). We tested typically developing emerging adults (18 to 25 years old) in both Cambridge face recognition tasks, an old-new face recognition task, and a car recognition task. Results indicate that the F-CFMT+ is a valid, internally consistent measure of unfamiliar face recognition that can be used alone or in tandem with the M-CFMT+ to assess recognition abilities for young adult White faces. When used together, performance on the F-CFMT+ and M-CFMT+ can be directly compared, adding to the ability to understand face recognition abilities for different kinds of faces. The two tasks have high convergent validity and relatively good divergent validity with car recognition in the same task paradigm. The F-CFMT+ will be useful to researchers interested in evaluating a broad range of questions about face recognition abilities in both typically developing individuals and those with atypical social information processing abilities.

Changes in Cortical Coherence Supporting Complex Visual and Social Processing in Adolescence.

Despite our differences, there is much about the natural visual world that most observers perceive in common. Across adults, approximately 30% of the brain is activated in a consistent fashion while viewing naturalistic input. At what stage of development is this consistency of neural profile across individuals present? Here, we focused specifically on whether this mature profile is present in adolescence, a key developmental period that bridges childhood and adulthood, and in which new cognitive and social challenges are at play. We acquired fMRI data evoked by a movie shown twice to younger (9-14 years old) and older adolescents (15-19 years old) and to adults, and conducted three key analyses. First, we characterized the consistency of the neural response within individuals (across separate runs of the movie), then within individuals of the same age group, and, last, between age groups. The neural consistency within individuals was similar across age groups with reliable activation in largely overlapping but slightly different cortical regions. In contrast, somewhat differing regions exhibited higher within-age correlations in both groups of adolescents than in the adults. Last, across the whole cortex, we identified regions evincing different patterns of maturation across age. Together, these findings provide a fine-grained characterization of functional neural development in adolescence and uncover signatures of widespread change in cortical coherence that supports the emerging mature stereotypical responses to naturalistic stimuli. These results also offer a more nuanced account of development that obeys neither a rigid linear progression nor a large qualitative change over time.

I know that voice! Mothers' voices influence children's perceptions of emotional intensity.

The ability to interpret others' emotions is a critical skill for children's socioemotional functioning. Although research has emphasized facial emotion expressions, children are also constantly required to interpret vocal emotion expressed at or around them by individuals who are both familiar and unfamiliar to them. The current study examined how speaker familiarity, specific emotions, and the acoustic properties that comprise affective prosody influenced children's interpretations of emotional intensity. Participants were 51 7- and 8-year-olds presented with speech stimuli spoken in happy, angry, sad, and nonemotional prosodies by both each child's mother and another child's mother unfamiliar to the target child. Analyses indicated that children rated their own mothers as more intensely emotional compared with the unfamiliar mothers and that this effect was specific to angry and happy prosodies. Furthermore, the acoustic properties predicted children's emotional intensity ratings in different patterns for each emotion. The results are discussed in terms of the significance of the mother's voice in children's development of emotional understanding.

Evaluating the organizational structure and specificity of network topology within the face processing system.

There is increasing appreciation that network-level interactions among regions produce components of face processing previously ascribed to individual regions. Our goals were to use an exhaustive data-driven approach to derive and quantify the topology of directed functional connections within a priori defined nodes of the face processing network and evaluate whether the topology is category-specific. Young adults were scanned with fMRI as they viewed movies of faces, objects, and scenes. We employed GIMME to model effective connectivity among core and extended face processing regions, which allowed us to evaluate all possible directional connections, under each viewing condition (face, object, place). During face processing, we observed directional connections from the right posterior superior temporal sulcus to both the right occipital face area and right fusiform face area (FFA), which does not reflect the topology reported in prior studies. We observed connectivity between core and extended regions during face processing, but this limited to a feed-forward connection from the FFA to the amygdala. Finally, the topology of connections was unique to face processing. These findings suggest that the pattern of directed functional connections within the face processing network, particularly in the right core regions, may not be as hierarchical and feed-forward as described previously. Our findings support the notion that topologies of network connections are specialized, emergent, and dynamically responsive to task demands.

Pubertal development shapes perception of complex facial expressions.

We previously hypothesized that pubertal development shapes the emergence of new components of face processing (Scherf et al., 2012; Garcia & Scherf, 2015). Here, we evaluate this hypothesis by investigating emerging perceptual sensitivity to complex versus basic facial expressions across pubertal development. We tested pre-pubescent children (6-8 years), age- and sex-matched adolescents in early and later stages of pubertal development (11-14 years), and sexually mature adults (18-24 years). Using a perceptual staircase procedure, participants made visual discriminations of both socially complex expressions (sexual interest, contempt) that are arguably relevant to emerging peer-oriented relationships of adolescence, and basic (happy, anger) expressions that are important even in early infancy. Only sensitivity to detect complex expressions improved as a function of pubertal development. The ability to perceive these expressions is adult-like by late puberty when adolescents become sexually mature. This pattern of results provides the first evidence that pubertal development specifically influences emerging affective components of face perception in adolescence.

The visual white matter: The application of diffusion MRI and fiber tractography to vision science.

Visual neuroscience has traditionally focused much of its attention on understanding the response properties of single neurons or neuronal ensembles. The visual white matter and the long-range neuronal connections it supports are fundamental in establishing such neuronal response properties and visual function. This review article provides an introduction to measurements and methods to study the human visual white matter using diffusion MRI. These methods allow us to measure the microstructural and macrostructural properties of the white matter in living human individuals; they allow us to trace long-range connections between neurons in different parts of the visual system and to measure the biophysical properties of these connections. We also review a range of findings from recent studies on connections between different visual field maps, the effects of visual impairment on the white matter, and the properties underlying networks that process visual information supporting visual face recognition. Finally, we discuss a few promising directions for future studies. These include new methods for analysis of MRI data, open datasets that are becoming available to study brain connectivity and white matter properties, and open source software for the analysis of these data.

From Caregivers to Peers: Puberty Shapes Human Face Perception.

Puberty prepares mammals to sexually reproduce during adolescence. It is also hypothesized to invoke a social metamorphosis that prepares adolescents to take on adult social roles. We provide the first evidence to support this hypothesis in humans and show that pubertal development retunes the face-processing system from a caregiver bias to a peer bias. Prior to puberty, children exhibit enhanced recognition for adult female faces. With puberty, superior recognition emerges for peer faces that match one's pubertal status. As puberty progresses, so does the peer recognition bias. Adolescents become better at recognizing faces with a pubertal status similar to their own. These findings reconceptualize the adolescent "dip" in face recognition by showing that it is a recalibration of the face-processing system away from caregivers toward peers. Thus, in addition to preparing the physical body for sexual reproduction, puberty shapes the perceptual system for processing the social world in new ways.

A theoretical rut: revisiting and critically evaluating the generalized under/over-connectivity hypothesis of autism.

In 2004, two papers proposed that pervasive functional under-connectivity (Just et al., ) or a trade-off between excessive local connectivity at the cost of distal under-connectivity (Belmonte et al., ) characterizes atypical brain organization in autism. Here, we take stock of the most recent and rigorous functional and structural connectivity findings with a careful eye toward evaluating the extent to which they support these original hypotheses. Indeed, the empirical data do not support them. From rsfMRI studies in adolescents and adults, there is an emerging consensus regarding long-range functional connections indicating cortico-cortical under-connectivity, specifically involving the temporal lobes, combined with subcortical-cortical over-connectivity. In contrast, there is little to no consensus regarding local functional connectivity or findings from task-based functional connectivity studies. The structural connectivity data suggest that white matter tracts are pervasively weak, particularly in the temporal lobe. Together, these findings are revealing how deeply complex the story is regarding atypical neural network organization in autism. In other words, distance and strength of connectivity as individual factors or as interacting factors do not consistently explain the patterns of atypical neural connectivity in autism. Therefore, we make several methodological recommendations and highlight developmental considerations that will help researchers in the field cultivate new hypotheses about the nature and mechanisms of potentially aberrant functional and structural connectivity in autism.

Animal, but not human, faces engage the distributed face network in adolescents with autism.

Multiple hypotheses have been offered to explain the impaired face-processing behavior and the accompanying underlying disruptions in neural circuitry among individuals with autism. We explored the specificity of atypical face-processing activation and potential alterations to fusiform gyrus (FG) morphology as potential underlying mechanisms. Adolescents with high functioning autism (HFA) and age-matched typically developing (TD) adolescents were scanned with sMRI and fMRI as they observed human and animal faces. In spite of exhibiting comparable face recognition behavior, the HFA adolescents evinced hypo-activation throughout the face-processing system in response to unfamiliar human, but not animal, faces. They also exhibited greater activation in affective regions of the face-processing network in response to animal, but not human, faces. Importantly, this atypical pattern of activation in response to human faces was not related to atypical structural properties of the FG. This atypical neural response to human faces in autism may stem from abnormalities in the ability to represent the reward value of social (i.e. conspecific) stimuli.

Size precedes view: developmental emergence of invariant object representations in lateral occipital complex.

Although object perception involves encoding a wide variety of object properties (e.g., size, color, viewpoint), some properties are irrelevant for identifying the object. The key to successful object recognition is having an internal representation of the object identity that is insensitive to these properties while accurately representing important diagnostic features. Behavioral evidence indicates that the formation of these kinds of invariant object representations takes many years to develop. However, little research has investigated the developmental emergence of invariant object representations in the ventral visual processing stream, particularly in the lateral occipital complex (LOC) that is implicated in object processing in adults. Here, we used an fMR adaptation paradigm to evaluate age-related changes in the neural representation of objects within LOC across variations in size and viewpoint from childhood through early adulthood. We found a dissociation between the neural encoding of object size and object viewpoint within LOC: by age of 5-10 years, area LOC demonstrates adaptation across changes in size, but not viewpoint, suggesting that LOC responses are invariant to size variations, but that adaptation across changes in view is observed in LOC much later in development. Furthermore, activation in LOC was correlated with behavioral indicators of view invariance across the entire sample, such that greater adaptation was correlated with better recognition of objects across changes in viewpoint. We did not observe similar developmental differences within early visual cortex. These results indicate that LOC acquires the capacity to compute invariance specific to different sources of information at different time points over the course of development.

Emerging structure-function relations in the developing face processing system.

To evaluate emerging structure-function relations in a neural circuit that mediates complex behavior, we investigated age-related differences among cortical regions that support face recognition behavior and the fiber tracts through which they transmit and receive signals using functional neuroimaging and diffusion tensor imaging. In a large sample of human participants (aged 6-23 years), we derived the microstructural and volumetric properties of the inferior longitudinal fasciculus (ILF), the inferior fronto-occipital fasciculus, and control tracts, using independently defined anatomical markers. We also determined the functional characteristics of core face- and place-selective regions that are distributed along the trajectory of the pathways of interest. We observed disproportionately large age-related differences in the volume, fractional anisotropy, and mean and radial, but not axial, diffusivities of the ILF. Critically, these differences in the structural properties of the ILF were tightly and specifically linked with an age-related increase in the size of a key face-selective functional region, the fusiform face area. This dynamic association between emerging structural and functional architecture in the developing brain may provide important clues about the mechanisms by which neural circuits become organized and optimized in the human cortex.

How is race perceived during adolescence? A meta-analysis of the own-race bias.

Adolescence is a critical developmental period that is marked by drastic changes in face recognition, which are reflected in patterns of bias (i.e., superior recognition for some individuals compared to others). Here, we evaluate how race is perceived during face recognition and whether adolescents exhibit an own-race bias (ORB). We conducted a Bayesian meta-analysis to estimate the summary effect size of the ORB across 16 unique studies (38 effect sizes) with 1,321 adolescent participants between the ages of ∼10-22 years of age. This meta-analytic approach allowed us to inform the analysis with prior findings from the adult literature and evaluate how well they fit the adolescent literature. We report a positive, small ORB (Hedges's g = 0.24) that was evident under increasing levels of uncertainty in the analysis. The magnitude of the ORB was not systematically impacted by participant age or race, which is inconsistent with predictions from perceptual expertise and social cognitive theories. Critically, our findings are limited in generalizability by the study samples, which largely include White adolescents in White-dominant countries. Future longitudinal studies that include racially diverse samples and measure social context, perceiver motivation, peer reorientation, social network composition, and ethnic-racial identity development are critical for understanding the presence, magnitude, and relative flexibility of the ORB in adolescence. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

Social visual attention as a treatment outcome: evaluating the social games for autistic adolescents (SAGA) intervention.

A core feature of autism involves difficulty perceiving and interpreting eye gaze shifts as nonverbal communicative signals. A hypothesis about the origins of this phenotype is that it emerges from developmentally different social visual attention (SVA). We developed Social Games for Autistic Adolescents (SAGA; Scherf et al. BMJ Open 8(9):e023682, 2018) as a serious game intervention for autistic individuals to discover the significance of eye gaze cues. Previously, we demonstrated the effectiveness of SAGA to improve the perception and understanding of eye gaze cues and social skills for autistic adolescents (Griffin et al. JCPP Adv 1(3):e12041, 2021). Here, we determine whether increases in social visual attention to faces and/or target gazed-at objects, as measured via eye tracking during the same Gaze Perception task in the same study sample, moderated this improvement. In contrast to predictions, SVA to faces did not differentially increase for the treatment group. Instead, both groups evinced a small increase in SVA to faces over time. Second, Prior to the SAGA intervention, attention to faces failed to predict performance in the Gaze Perception task for both the treatment and standard care control groups. However, at post-test, autistic adolescents in the treatment group were more likely to identify the object of directed gaze when they attended longer to faces and longer to target objects. Importantly, this is the first study to measure social visual attention via eye tracking as a treatment response in an RCT for autism. NCT02968225.

The amygdala: an agent of change in adolescent neural networks.

This article is part of a Special Issue "Puberty and Adolescence". A unique component of adolescent development is the need to master new developmental tasks in which peer interactions become primary (for the purposes of becoming autonomous from parents, forming intimate friendships, and romantic/sexual partnerships). Previously, it has been suggested that the ability to master these tasks requires an important re-organization in the relation between perceptual, motivational, affective, and cognitive systems in a very general and broad way that is fundamentally influenced by the infusion of sex hormones during pubertal development (Scherf et al., 2012). Herein, we extend this argument to suggest that the amygdala, which is vastly connected with cortical and subcortical regions and contains sex hormone receptors, may lie at the heart of this re-organization. We propose that during adolescent development there is a shift in the attribution of relevance to existing stimuli and contexts that is mediated by the amygdala (e.g., heightened relevance of peer faces, reduced relevance of physical distance from parents). As a result, amygdala inputs to existing stable neural networks are re-weighted (increased or decreased), which destabilizes the functional interactions among regions within these networks and allows for a critical restructuring of the network functional organization. This process of network re-organization enables processing of qualitatively new kinds of social information and the emergence of novel behaviors that support mastery of adolescent-specific developmental tasks.

Experimental Therapeutics: Opportunities and Challenges Stemming From the National Institute of Mental Health Workshop on Novel Target Discovery and Psychosocial Intervention Development.

There has been slow progress in the development of interventions that prevent and/or reduce mental-health morbidity and mortality. The National Institute of Mental Health (NIMH) launched an experimental-therapeutics initiative with the goal of accelerating the development of effective interventions. The emphasis is on interventions designed to engage a target mechanism. A target mechanism is a process (e.g., behavioral, neurobiological) proposed to underlie change in a defined clinical endpoint and through change in which an intervention exerts its effect. This article is based on discussions from an NIMH workshop conducted in February 2020 and subsequent conversations among researchers using this approach. We discuss the components of an experimental-therapeutics approach such as clinical-outcome selection, target definition and measurement, intervention design and selection, and implementation of a team-science strategy. We emphasize the important contributions of different constituencies (e.g., patients, caregivers, providers) in deriving hypotheses about novel target mechanisms. We highlight strategies for target-mechanism identification using published and hypothetical examples. We consider the decision-making dilemmas that arise with different patterns of results in purported mechanisms and clinical outcomes. We end with considerations of the practical challenges of this approach and the implications for future directions of this initiative.

"What" precedes "which": developmental neural tuning in face- and place-related cortex.

Although category-specific activation for faces in the ventral visual pathway appears adult-like in adolescence, recognition abilities for individual faces are still immature. We investigated how the ability to represent "individual" faces and houses develops at the neural level. Category-selective regions of interest (ROIs) for faces in the fusiform gyrus (FG) and for places in the parahippocampal place area (PPA) were identified individually in children, adolescents, and adults. Then, using an functional magnetic resonance imaging adaptation paradigm, we measured category selectivity and individual-level adaptation for faces and houses in each ROI. Only adults exhibited both category selectivity and individual-level adaptation bilaterally for faces in the FG and for houses in the PPA. Adolescents showed category selectivity bilaterally for faces in the FG and houses in the PPA. Despite this profile of category selectivity, adolescents only exhibited individual-level adaptation for houses bilaterally in the PPA and for faces in the "left" FG. Children only showed category-selective responses for houses in the PPA, and they failed to exhibit category-selective responses for faces in the FG and individual-level adaptation effects anywhere in the brain. These results indicate that category-level neural tuning develops prior to individual-level neural tuning and that face-related cortex is disproportionately slower in this developmental transition than is place-related cortex.

Connecting developmental trajectories: biases in face processing from infancy to adulthood.

The nature of the developmental trajectory of face recognition abilities from infancy through adulthood is multifaceted and currently not well understood. We argue that the understanding of this trajectory can be greatly informed by taking a more functionalist approach in which the influence of age-appropriate developmental tasks and goals are considered. To build this argument, we provide a focused review of developmental change across several important biases within face processing (species, race, age, and gender biases) from infancy through adulthood. We show that no existing theoretical framework can simultaneously and parsimoniously explain these very different trajectories and relative degrees of plasticity. We offer several examples of infant- and adolescent-specific developmental tasks that we predict have an essential influence on the content and description of information that individuals need to extract from faces at these very different developmental stages. Finally, we suggest that this approach may provide a unique opportunity to study the role of early experience in (i.e., age of acquisition effects) and the quality and range of experiences that are critical for shaping behaviors through the course of development, from infancy to adulthood.

College as a Developmental Context for Emerging Adulthood in Autism: A Systematic Review of What We Know and Where We Go from Here.

Autistic individuals often struggle to successfully navigate emerging adulthood (EA). College is an increasingly common context in which individuals learn and hone the necessary skills for adulthood. The goal of this paper is to systematically review and assess the existing research on college as a context of EA development in autistic individuals, particularly in terms of understanding whether and how this context might be critically different for those who are typically developing or developing with other disabilities. Our findings indicate that ASD college students report feeling prepared academically, but exhibit weaknesses in daily living and social skills. Interventions largely focus on social skills, and rarely evaluate outcomes relevant to college success or longer-term emerging adulthood independence. We conclude with hypotheses and recommendations for future work that are essential for understanding and supporting ASD students as they navigate potentially unique challenges in college and their transition to independence during EA.

A quantitative meta-analysis of face recognition deficits in autism: 40 years of research.

The ability to recognize an individual face is essential to human social interaction. Even subtle errors in this process can have huge implications for the way we relate to social partners. Because autism spectrum disorder (ASD) is characterized by deficits in social interaction, researchers have theorized about the potential role of atypical face identity processing to the symptom profile of ASD for more than 40 years. We conducted an empirical meta-analysis of this large literature to determine whether and to what extent face identity processing is atypical in ASD compared to typically developing (TD) individuals. We also tested the hypotheses that the deficit is selective to face identity recognition, not perception, and that methodological variation across studies moderates the magnitude of the estimated deficit. We identified 112 studies (5,390 participants) that generated 172 effect sizes from both recognition (k = 119) and discrimination (k = 53) paradigms. We used state-of-the-art approaches for assessing the validity and robustness of the analyses. We found comparable and large deficits in ASD for both face identity recognition (Hedge's g = -0.86) and discrimination (Hedge's g = -0.82). This means that the score of an average ASD individual is nearly 1 SD below the average TD individual on tasks assessing both aspects of face identity processing. These deficits generalize across age groups, sex, IQ scores, and task paradigms. These findings suggest that deficits in face identity processing may represent a core deficit in ASD. (PsycInfo Database Record (c) 2021 APA, all rights reserved).