Putting people in context: ERP responses to bodies in natural scenes.

The N190 is a body-sensitive ERP component that responds to images of human bodies in different poses. In natural settings, bodies vary in posture and appear within complex, cluttered environments, frequently with other people. In many studies, however, such variability is absent. How does the N190 response change when observers see images that incorporate these sources of variability? In two experiments (N = 16 each), we varied the natural appearance of upright and inverted bodies to examine how the N190 amplitude, latency, and the Body-Inversion Effect (BIE) were affected by natural variability. In Experiment 1, we varied the number of people present in upright and inverted naturalistic scenes such that only one body, a subitizable number of bodies, or a "crowd" was present. In Experiment 2, we varied the natural body appearance by presenting bodies either as silhouettes or with photographic detail. Further, we varied the natural background appearance by either removing it or presenting individual bodies within a rich environment. Using component-based analyses of the N190, we found that the number of bodies in a scene reduced the N190 amplitude, but didn't affect the BIE (Experiment 1). Naturalistic body and background appearance (Experiment 2) also affected the N190, such that component amplitude was dramatically reduced by naturalistic appearance. To complement this analysis, we examined the contribution of spatiotemporal features (i.e., electrode × time point amplitude) via SVM decoding. This technique allows us to examine which timepoints across the entire waveform contribute the most to successful decoding of body orientation in each condition. This analysis revealed that later timepoints (after 300ms) contribute most to successful orientation decoding. These results demonstrate that natural appearance variability affects body processing at the N190 and that later ERP components may make important contributions to body processing in natural scenes.

Sensitivity to face animacy and inversion in childhood: Evidence from EEG data.

Adults exhibit relative behavioral difficulties in processing inanimate, artificial faces compared to real human faces, with implications for using artificial faces in research and designing artificial social agents. However, the developmental trajectory of inanimate face perception is unknown. To address this gap, we used electroencephalography to investigate inanimate faces processing in cross-sectional groups of 5-10-year-old children and adults. A face inversion manipulation was used to test whether face animacy processing relies on expert face processing strategies. Groups of 5-7-year-olds (N = 18), 8-10-year-olds (N = 18), and adults (N = 16) watched pictures of real or doll faces presented in an upright or inverted orientation. Analyses of event-related potentials revealed larger N170 amplitudes in response to doll faces, irrespective of age group or face orientation. Thus, the N170 is sensitive to face animacy by 5-7 years of age, but such sensitivity may not reflect high-level, expert face processing. Multivariate pattern analyses of the EEG signal additionally assessed whether animacy information could be reliably extracted during face processing. Face orientation, but not face animacy, could be reliably decoded from occipitotemporal channels in children and adults. Face animacy could be decoded from whole scalp channels in adults, but not children. Together, these results suggest that 5-10-year-old children exhibit some sensitivity to face animacy over occipitotemporal regions that is comparable to adults.

Neural sensitivity to natural image statistics changes during middle childhood.

Natural images have properties that adults' behavioral and neural responses are sensitive to, but the development of this sensitivity is not clear. Behaviorally, children acquire adult-like sensitivity to natural image statistics during middle childhood (Ellemberg et al., 2012), but infants exhibit sensitivity to deviations of natural image structure (Balas & Woods, 2014). We used event-related potentials (ERPs) to examine sensitivity to natural image statistics during childhood at distinct processing stages (the P1 and N1 components). We presented children (5-10 years old) and adults with natural images varying in positive/negative contrast, and natural/synthetic texture appearance to compare electrophysiological responses to images that did or did not violate natural statistics. We hypothesized that children would acquire sensitivity to these deviations late in middle childhood. Instead, we observed significant responses to unnatural contrast and texture statistics at the N1 in all age groups. At the P1, however, only young children exhibited sensitivity to contrast polarity. The latter effect suggests greater sensitivity earlier in development to some violations of natural image statistics. We discuss these results in terms of changing patterns of invariant texture processing during middle childhood and ongoing refinement of the representations supporting natural image perception.

Children are sensitive to mutual information in intermediate-complexity face and non-face features.

Understanding developmental changes in children's use of specific visual information for recognizing object categories is essential for understanding how experience shapes recognition. Research on the development of face recognition has focused on children's use of low-level information (e.g. orientation sub-bands), or high-level information. In face categorization tasks, adults also exhibit sensitivity to intermediate complexity features that are diagnostic of the presence of a face. Do children also use intermediate complexity features for categorizing faces and objects, and, if so, how does their sensitivity to such features change during childhood? Intermediate-complexity features bridge the gap between low- and high-level processing: they have computational benefits for object detection and segmentation, and are known to drive neural responses in the ventral visual system. Here, we have investigated the developmental trajectory of children's sensitivity to diagnostic category information in intermediate-complexity features. We presented children (5-10 years old) and adults with image fragments of faces (Experiment 1) and cars (Experiment 2) varying in their mutual information, which quantifies a fragment's diagnosticity of a specific category. Our goal was to determine whether children were sensitive to the amount of mutual information in these fragments, and if their information usage is different from adults. We found that despite better overall categorization performance in adults, all children were sensitive to fragment diagnosticity in both categories, suggesting that intermediate representations of appearance are established early in childhood. Moreover, children's usage of mutual information was not limited to face fragments, suggesting the extracting intermediate-complexity features is a process that is not specific only to faces. We discuss the implications of our findings for developmental theories of face and object recognition.

Neural Sensitivity to Mutual Information in Intermediate-Complexity Face Features Changes during Childhood.

One way in which face recognition develops during infancy and childhood is with regard to the visual information that contributes most to recognition judgments. Adult face recognition depends on critical features spanning a hierarchy of complexity, including low-level, intermediate, and high-level visual information. To date, the development of adult-like information biases for face recognition has focused on low-level features, which are computationally well-defined but low in complexity, and high-level features, which are high in complexity, but not defined precisely. To complement this existing literature, we examined the development of children's neural responses to intermediate-level face features characterized using mutual information. Specifically, we examined children's and adults' sensitivity to varying levels of category diagnosticity at the P100 and N170 components. We found that during middle childhood, sensitivity to mutual information shifts from early components to later ones, which may indicate a critical restructuring of face recognition mechanisms that takes place over several years. This approach provides a useful bridge between the study of low- and high-level visual features for face recognition and suggests many intriguing questions for further investigation.

Neural sensitivity to natural texture statistics in infancy.

During infancy, vision becomes tuned to environmental statistics. For example, infant face recognition "narrows" in response to the frequency of face categories in the visual world, inducing out-group effects that disadvantage other-race, other-species, and other-age face recognition. There are many other low-level statistical regularities in visual experience that infants may also become tuned to during this period. In particular, natural scenes have lawful properties that adults and children are sensitive to. To what extent do infants become tuned to these regularities during the first year of life? In particular, do infants exhibit evidence of perceptual narrowing that excludes atypical images from fluent processing? We examined this question by measuring 6- and 9-month-old infants' event-related potentials (ERPs) to natural and artificial textures created by: (a) Disrupting local statistics via contrast negation, (b) Disrupting global statistics via parametric texture synthesis, or (c) both of these. We predicted that younger infants' would be sensitive to both manipulations of natural appearance, but that older infants might not distinguish between different kinds of atypical images. Instead, we found that sensitivity to synthetic appearance is only evident late in infancy. We discuss what these results imply for our understanding of visual statistical learning in infancy.

School-age children's neural sensitivity to horizontal orientation energy in faces.

Face processing mechanisms are tuned to specific low-level features including mid-range spatial frequencies and horizontal orientation energy. Behaviorally, adult observers are more effective at face recognition tasks when these information channels are available. Neural responses to face images also reflect these information biases: Face-sensitive ERP components respond preferentially to face images that contain horizontal orientation energy. How does neural tuning of face representations to horizontal information develop? Behavioral results show that this information bias increases over time such that younger children have a reduced bias favoring horizontally-filtered faces that increases with age. In the present study, we chose to investigate how neural sensitivity to these low-level features develops in the same age range, using ERP as a means of studying children and adults. Specifically, we examined how both face-sensitive ERP components (the P100 and N170) changed their responses to faces and non-faces as a function of age and orientation energy. Briefly, we found that the latency of the P100 and N170 component across age groups was consistent with the gradual emergence of a bias favoring horizontal orientation energy during middle childhood. The amplitude of the N170 component, however, exhibited a more complicated developmental profile that does not easily map onto previous behavioral results obtained from children in the same age ranges.

The Impact of Face Inversion on Animacy Categorization.

Face animacy perception is categorical: Gradual changes in the real/artificial appearance of a face lead to nonlinear behavioral responses. Neural markers of face processing are also sensitive to face animacy, further suggesting that these are meaningful perceptual categories. Artificial faces also appear to be an "out-group" relative to real faces such that behavioral markers of expert-level processing are less evident with artificial faces than real ones. In the current study, we examined how categorical processing of real versus doll faces was impacted by the face inversion effect, which is one of the most robust markers of expert face processing. We examined how explicit categorization of faces drawn from a real/doll morph continuum was affected by face inversion (Experiment 1) and also how the response properties of the N170 were impacted by face animacy and inversion. We found that inversion does not change the position or steepness of the category boundary measured behaviorally. Further, neural markers of face processing are equally impacted by inversion regardless of whether they are elicited by real faces or doll faces. On balance, our results indicate that inversion has a limited impact on the categorical perception of face animacy.

Hometown size affects the processing of naturalistic face variability.

Face exposure during development determines adults' abilities to recognize faces and the information they use to process them. Individual differences in the face categories represented in the visual environment can lead to category-specific deficits for recognizing faces that are atypical of observer's experience (e.g. the other-race effect). But what happens when observers have limited opportunities to learn about faces in general? In previous work, we found that observers from depopulated areas have poorer face recognition performance than observers from larger communities, suggesting that impoverished face experience limits face processing broadly. Here, we further investigate this phenomenon by examining how hometown size impacts the ability to assess appearance variability in natural images of faces and bodies. We asked individuals from small and large communities to complete (1) an unconstrained card-sorting task designed to test observers' ability to categorize within-person and between-person appearance variability properly, and (2) the Cambridge Face Memory Test. For both tasks, we examined the direct comparison between groups as well as the relationship between CFMT scores and sorting performance as a function of face experience. We find that small-town observers perform more poorly on the CFMT, but exhibit both better and worse performance than large-town observers on different aspects of the card-sorting task. Further, we also examine the relationship between CFMT performance and card-sorting errors. Our results suggest that individual differences in lifetime face exposure induce important variation in face processing abilities.

Orientation biases for facial emotion recognition during childhood and adulthood.

Facial emotion recognition develops slowly, with continuing changes in performance observable up to 10 years of age and beyond. In the current study, we chose to examine how the use of specific low-level visual features for emotion recognition may change during childhood. Adults exhibit information biases for face recognition; specific spatial frequency and orientation sub-bands make a larger contribution to recognition than others. This means that depending on the specific task (e.g., identification, emotion recognition), participants will perform worse when some features are removed from the original image and better when those features are included. One example of such an information bias for face recognition is the differential contribution of horizontal orientation energy relative to vertical orientation energy; adult participants are better able to recognize faces and categorize their emotional expressions when horizontal information is included than when only vertical information is included. Although several recent studies have demonstrated various ways in which horizontal orientation energy (and so-called "bar-codes" for face appearance) contribute to adult face processing, there have been as yet no studies describing how such a bias emerges developmentally that may offer insight into the mechanisms underlying the slow development of facial emotion recognition. In the current study, we compared children's (5- and 6-year-olds and 7- and 8-year-olds) and adults' performance in a simple emotion categorization task using orientation-filtered faces to determine the extent to which horizontal and vertical orientation energy contributed to recognition as a function of age. We found that although all three participant groups exhibited a clear bias favoring the use of horizontal orientation energy, the nature of this bias differed as a function of age. Specifically, 5- and 6-year-olds exhibited a disproportionate performance cost when vertical orientation energy was all that was available relative to when stimuli were limited to horizontal orientation energy. One feature of the development of facial emotion recognition, thus, appears to be the capability to use suboptimal or weakly diagnostic information to support recognition.

A face detection bias for horizontal orientations develops in middle childhood.

Faces are complex stimuli that can be described via intuitive facial features like the eyes, nose, and mouth, "configural" features like the distances between facial landmarks, and features that correspond to computations performed in the early visual system (e.g., oriented edges). With regard to this latter category of descriptors, adult face recognition relies disproportionately on information in specific spatial frequency and orientation bands: many recognition tasks are performed more accurately when adults have access to mid-range spatial frequencies (8-16 cycles/face) and horizontal orientations (Dakin and Watt, 2009). In the current study, we examined how this information bias develops in middle childhood. We recruited children between the ages of 5-10 years-old to participate in a simple categorization task that required them to label images according to whether they depicted a face or a house. Critically, children were presented with face and house images comprised either of primarily horizontal orientation energy, primarily vertical orientation energy, or both horizontal and vertical orientation energy. We predicted that any bias favoring horizontal information over vertical should be more evident in faces than in houses, and also that older children would be more likely to show such a bias than younger children. We designed our categorization task to be sufficiently easy that children would perform at near-ceiling accuracy levels, but with variation in response times that would reflect how they rely on different orientations as a function of age and object category. We found that horizontal bias for face detection (but not house detection) correlated significantly with age, suggesting an emergent category-specific bias for horizontal orientation energy that develops during middle childhood. These results thus suggest that the tuning of high-level recognition to specific low-level visual features takes place over several years of visual development.

N170 face specificity and face memory depend on hometown size.

Face recognition depends on visual experience in a number of different ways. Infrequent exposure to faces belonging to categories defined by species, age, or race can lead to diminished memory for and discrimination between members of those categories relative to faces belonging to categories that dominate an observer's environment. Early visual impairment can also have long-lasting and broad effects on face discrimination - just a few months of visual impairment due to congenital cataracts can lead to diminished discrimination between faces that differ in their configuration, for example (Le Grand et al., 2001). Presently, we consider a novel aspect of visual experience that may impact face recognition: The approximate amount of different faces observers encountered during their childhood. We recruited undergraduate observers from small (500-1000 individuals) and large communities (30,000-100,000 individuals) and asked them to complete a standard face memory test and a basic ERP paradigm designed to elicit a robust N170 response, including the classic face inversion effect. We predicted that growing up in a small community might lead to diminished face memory and an N170 response that was less specific to faces. These predictions were confirmed, suggesting that the sheer number of faces one can interact with during their upbringing shapes their behavioral abilities and the functional architecture of face processing in the brain.

Detecting personal familiarity depends on static frames in "thin slices" of behavior.

Brief glimpses of nonverbal behavior (or "thin slices") offer ample visual information to make reliable judgments about individuals. Previous work has largely focused on the personality characteristics and traits of individuals; however, the nature of dyadic relationships (strangers, lovers, or friends) can also be determined (Ambady & Gray, Journal of Personality and Social Psychology, 83, 947-961 2002). Judgments from thin slices are known to be accurate, but the motion features supporting accurate performance are unknown. We explored whether personal familiarity was detectable within the context of "thin slices" of genuine interaction, as well as the invariant properties of thin-slice recognition. In two experiments, participants sequentially viewed two 6-s silent videos on each trial of an individual interacting with an unfamiliar partner; the other depicted the same person interacting with a personally familiar partner. All sequences were cropped so that only the target individual was visible. In Experiment 1, participants viewed either the original sequences, reversed sequences, a static-image "slideshow" of the sequence, or a static-image slideshow with blank frames separating the images. In Experiment 2, all participants viewed the original sequences and clips played at either double speed or half speed. Participants' performance was above chance in the forward and reverse conditions, but was significantly better in both the static-image slideshow conditions. When task speed was manipulated, we found a larger performance cost for fast than for slow videos. Detecting personal familiarity via spontaneous natural gestures depends on information in static images more than on face or body movement. Although static images are typically less important for recognizing nonverbal behavior, we argue they may be valuable for making familiarity judgments from thin slices.

Reflexive orienting in response to short- and long-duration gaze cues in young, young-old, and old-old adults.

Shifting visual focus on the basis of the perceived gaze direction of another person is one form of joint attention. In the present study, we investigated whether this socially relevant form of orienting is reflexive and whether it is influenced by age. Green and Woldorff (Cognition 122:96-101, 2012) argued that rapid cueing effects (i.e., faster responses to validly than to invalidly cued targets) were limited to conditions in which a cue overlapped in time with a target. They attributed slower responses following invalid cues to the time needed to resolve the incongruent spatial information provided by the concurrently presented cue and target. In the present study, we examined the orienting responses of young (18-31 years), young-old (60-74 years), and old-old (75-91 years) adults following uninformative central gaze cues that overlapped in time with the target (Exp. 1) or that were removed prior to target presentation (Exp. 2). When the cue and target overlapped, all three groups localized validly cued targets more quickly than invalidly cued targets, and validity effects emerged earlier for the two younger groups (at 100 ms post-cue-onset) than for the old-old group (at 300 ms post-cue-onset). With a short-duration cue (Exp. 2), validity effects developed rapidly (by 100 ms) for all three groups, suggesting that validity effects resulted from reflexive orienting based on the gaze cue information rather than from cue-target conflict. Thus, although old-old adults may be slow to disengage from persistent gaze cues, attention continues to be reflexively guided by gaze cues late in life.

Timing of reflexive visuospatial orienting in young, young-old, and old-old adults.

This study examined adult age differences in reflexive orienting to two types of uninformative spatial cues: central arrows and peripheral onsets. In two experiments using a Posner cuing task, young adults (ages 18-28 years), young-old adults (60-74 years), and old-old adults (75-92 years) responded to targets that were preceded 100-1,000 ms earlier by a central arrow or a peripheral abrupt onset. In Experiment 1, the cue remained present upon target onset. Facilitation effects at short cue-target stimulus onset asynchronies (SOAs) were prolonged in duration for the two older groups relative to the young adults. At longer cue-target SOAs, inhibition of return (IOR) that was initiated by peripheral onset cues was observed in the performance of young adults but not in that of the two older groups. In Experiment 2, the cue was presented briefly and removed prior to target onset. The change in cue duration minimized age differences (particularly for young-old adults) in facilitation effects and led to IOR for all three age groups. The findings are consistent with the idea that attentional control settings change with age, with higher settings for older adults leading to delayed disengagement from spatial cues.

Spatial distribution of attentional inhibition is not altered in healthy aging.

Inhibition of return (IOR) is a phenomenon of attentional orienting that is indexed by slower responses to targets presented at previously attended locations. The purpose of this study was to examine adult age differences in the distribution of IOR to multiple locations. In three experiments, young adults (ages 18-30 years) and older adults (ages 60-87 years) completed an IOR task that varied in the number of simultaneous onset cues (one to seven) and the number of display locations (four or eight). Analyses were conducted to explore whether IOR patterns were most consistent with limited inhibitory resources, with regional distribution of inhibition, or with vector averaging of cues. The IOR effects were most consistent with vector averaging, such that multiple cues initiated a directional gradient of inhibition centered on the average direction of the cues. The IOR patterns varied minimally with age, consistent with the conclusion that older adults and young adults distributed inhibition in a similar manner.

Adult age differences in attention to semantic context.

In three experiments age differences in attention to semantic context were examined. The performance of younger adults (ages 18-29 years) and older adults (ages 60-79 years) on a semantic priming task indicated that both age groups could use information regarding the probability that a prime and target would be related to flexibly anticipate the target category given the prime word (Experiment 1). The timing by which target expectancies were reflected in reaction time performance was delayed for older adults as compared to younger adults, but only when the target was expected to be semantically unrelated to the prime word (Experiment 2). When the target and prime were expected to be semantically related, the time course of priming effects was similar for younger and older adults (Experiment 3). Together the findings indicate that older adults are able to use semantic context and the probability of stimulus relatedness to anticipate target information. Although aging may be associated with a delay in the timing by which controlled expectancies are expressed, these findings argue against an age-related decline in the ability to represent contextual information.

The emotional blink: adult age differences in visual attention to emotional information.

To assess age differences in attention-emotion interactions, the authors asked young adults (ages 18-33 years) and older adults (ages 60-80 years) to identify target words in a rapid serial visual presentation (RSVP) task. The second of two target words was neutral or emotional in content (positive in Experiment 1, negative in Experiment 2). In general, the ability to identify targets from a word stream declined with age. Age differences specific to the attentional blink were greatly reduced when baseline detection accuracy was equated between groups. With regard to emotion effects, older adults showed enhanced identification of both positive and negative words relative to neutral words, whereas young adults showed enhanced identification of positive words and reduced identification of negative words. Together these findings suggest that the nature of attention-emotion interactions changes with age, but there was little support for a motivational shift consistent with emotional regulation goals at an early stage of cognitive processing.

Aging and temporal patterns of inhibition of return.

Inhibition of return (IOR), an inhibitory component of spatial attention that is thought to bias visual search toward novel locations, is considered relatively well preserved with normal aging. We conducted two experiments to assess age-related changes in the temporal pattern of IOR. Inhibitory effects, which were strongly reflected in the performance of both younger adults (ages 18-34 years) and older adults (ages 60-79 years), diminished over a period of 5 s. The time point at which IOR began to diminish was delayed by approximately 1 s for older adults compared with younger adults; this pattern was observed on both a target detection task (Experiment 1) and a color discrimination task (Experiment 2). The finding that timing characteristics of IOR are altered by normal aging has potential implications for the manner in which inhibition aids search performance.