Elizabeth Simpson | University of Miami (original) (raw)

Research Papers by Elizabeth Simpson

Behavior Research Methods, 2023

Remote eye tracking with automated corneal reflection provides insights into the emergence and de... more Remote eye tracking with automated corneal reflection provides insights into the emergence and development of cognitive, social, and emotional functions in human infants and non-human primates. However, because most eye-tracking systems were designed for use in human adults, the accuracy of eye-tracking data collected in other populations is unclear, as are potential approaches to minimize measurement error. For instance, data quality may differ across species or ages, which are necessary considerations for comparative and developmental studies. Here we examined how the calibration method and adjustments to areas of interest (AOIs) of the Tobii TX300 changed the mapping of fixations to AOIs in a cross-species longitudinal study. We tested humans (N = 119) at 2, 4, 6, 8, and 14 months of age and macaques (Macaca mulatta; N = 21) at 2 weeks, 3 weeks, and 6 months of age. In all groups, we found improvement in the proportion of AOI hits detected as the number of successful calibration points increased, suggesting calibration approaches with more points may be advantageous. Spatially enlarging and temporally prolonging AOIs increased the number of fixation-AOI mappings, suggesting improvements in capturing infants' gaze behaviors; however, these benefits varied across age groups and species, suggesting different parameters may be ideal, depending on the population studied. In sum, to maximize usable sessions and minimize measurement error, eye-tracking data collection and extraction approaches may need adjustments for the age groups and species studied. Doing so may make it easier to standardize and replicate eye-tracking research findings.

Autism Research, 2020

Previous studies report prolonged auditory brainstem response (ABR) in children and adults with a... more Previous studies report prolonged auditory brainstem response (ABR) in children and adults with autism spectrum disorder (ASD). Despite its promise as a biomarker, it is unclear whether healthy newborns who later develop ASD also show ABR abnormalities. In the current study, we extracted ABR data on 139,154 newborns from their Universal Newborn Hearing Screening, including 321 newborns who were later diagnosed with ASD. We found that the ASD newborns had significant prolongations of their ABR phase and V-negative latency compared with the non-ASD newborns. Newborns in the ASD group also exhibited greater variance in their latencies compared to previous studies in older ASD samples, likely due in part to the low intensity of the ABR stimulus. These findings suggest that newborns display neurophysiologi-cal variation associated with ASD at birth. Future studies with higher-intensity stimulus ABRs may allow more accurate predictions of ASD risk, which could augment the universal ABR test that currently screens millions of newborns worldwide. Autism Res 2020, 00: 1-7. Lay Summary: Children with autism spectrum disorder (ASD) have slow brain responses to sounds. We examined these brain responses from newborns' hearing tests and found that newborns who were later diagnosed with autism also had slower brain responses to sounds. Future studies might use these findings to better predict autism risk, with a hearing test that is already used on millions of newborns worldwide.

Japanese Psychological Review, 2019

The field of primate cognition studies how primates, including humans, perceive, process, store, ... more The field of primate cognition studies how primates, including humans, perceive, process, store, retrieve, and use information to guide decision making and other behavior. Much of this research is motivated by a desire to understand how these abilities evolved. Large and diverse samples from a wide range of species are vital to achieving this goal. In reality, however, primate cognition research suffers from small sample sizes and is often limited to a handful of species, which constrains the evolutionary inferences we can draw. We conducted a systematic review of primate cognition research published between 2014 and 2019 to quantify the extent of this problem. Across 574 studies, the median sample size was 7 individuals. Less than 15% of primate species were studied at all, and only 19% of studies included more than one species. Further, the species that were studied varied widely in how much research attention they received, partly because a small number of test sites contributed most of the studies. These results suggest that the generalizability of primate cognition studies may be severely limited. Publication bias, questionable research practices, and a lack of replication attempts may exacerbate these problems. We describe the ManyPrimates project as one approach to overcoming some of these issues by establishing an infrastructure for large-scale collaboration in primate cognition research. Building on similar initiatives in other areas of psychology, this approach has already yielded one of the largest and most diverse primate samples to date and enables us to ask many research questions that can only be addressed through collaboration.

PLOS ONE, 2019

Infant temperament is theorized to lay the foundation for adult personality; however, many questi... more Infant temperament is theorized to lay the foundation for adult personality; however, many questions remain regarding personality in infancy, including the number of dimensions, extent to which they are adult-like, and their relation to other outcomes, such as mental and physical health. Here we tested whether adult-like personality dimensions are already present in infancy in a nonhuman primate species. We measured personality and subjective well-being in 7-month-old rhesus macaques (N = 55) using the Hominoid Personality Questionnaire and Subjective Well-Being Questionnaire, both of which were developed for adult primates based on human measures. Multiple human raters, who provided infants with daily care since birth, independently rated each infant. We found high inter-rater reliability. Results from a parallel analysis and scree plot indicated a five component structure, which, using principal components analysis, we found to be comprised of dimensions relating to Openness (e.g., curiosity, inquisitive, playfulness), Assertiveness (e.g., dominance, bullying, aggressive), Anxiety (e.g., vigilance, fearful), Friendliness (e.g., sociable, affectionate, sympathetic), and Intellect (e.g., organized, not erratic). These components are largely analogous to those in adult macaques, suggesting remarkably stable structural personality components across the lifespan. Infant macaques’ subjective well-being positively correlates with Openness and Assertiveness and negatively correlated with Anxiety, similar to findings in adult macaques and other primates. Together, these findings suggest that, in macaques, infant personality dimensions may be conceptually related to adult personality and challenge the view that infant temperament may be disorganized and not as meaningful as adult personality. Further research is necessary to explore the antecedents, predictive validity, and stability of these personality components across situations and with development.

Developmental Science, 2020

Humans detect faces efficiently from a young age. Face detection is critical for infants to ident... more Humans detect faces efficiently from a young age. Face detection is critical for infants to identify and learn from relevant social stimuli in their environments. Faces with eye contact are an especially salient stimulus, and attention to the eyes in infancy is linked to the emergence of later sociality. Despite the importance of both of these early social skills—attending to faces and attending to the eyes—surprisingly little is known about how they interact. We used eye tracking to explore whether eye contact influences infants' face detection. Longitudinally, we examined 2‐, 4‐, and 6‐month‐olds' (N = 65) visual scanning of complex image arrays with human and animal faces varying in eye contact and head orientation. Across all ages, infants displayed superior detection of faces with eye contact; however, this effect varied as a function of species and head orientation. Infants were more attentive to human than animal faces and were more sensitive to eye and head orientation for human faces compared to animal faces. Unexpectedly, human faces with both averted heads and eyes received the most attention. This pattern may reflect the early emergence of gaze following—the ability to look where another individual looks—which begins to develop around this age. Infants may be especially interested in averted gaze faces, providing early scaffolding for joint attention. This study represents the first investigation to document infants' attention patterns to faces systematically varying in their attentional states. Together, these findings suggest that infants develop early, specialized functional conspecific face detection.

Advances in Methods and Practices in Psychological Science, 2020

Psychological scientists have become increasingly concerned with issues related to methodology an... more Psychological scientists have become increasingly concerned with issues related to methodology and replicability, and infancy researchers in particular face specific challenges related to replicability: For example, high-powered studies are difficult to conduct, testing conditions vary across labs, and different labs have access to different infant populations. Addressing these concerns, we report on a large-scale, multisite study aimed at (a) assessing the overall replicability of a single theoretically important phenomenon and (b) examining methodological, cultural, and developmental moderators. We focus on infants’ preference for infant-directed speech (IDS) over adult-directed speech (ADS). Stimuli of mothers speaking to their infants and to an adult in North American English were created using semi-naturalistic laboratory-based audio recordings. Infants’ relative preference for IDS and ADS was assessed across 67 laboratories in North America, Europe, Australia, and Asia using the three common methods for measuring infants’ discrimination (head-turn preference, central fixation, and eye tracking). The overall meta-analytic effect size (Cohen’s d) was 0.35, 95% confidence interval = [0.29, 0.42], which was reliably above zero but smaller than the meta-analytic mean computed from previous literature (0.67). The IDS preference was significantly stronger in older children, in those children for whom the stimuli matched their native language and dialect, and in data from labs using the head-turn preference procedure. Together, these findings replicate the IDS preference but suggest that its magnitude is modulated by development, native-language experience, and testing procedure.

Developmental Psychobiology, 2020

The present study explored behavioral norms for infant social attention in typically developing h... more The present study explored behavioral norms for infant social attention in typically developing human and nonhuman primate infants. We examined the normative development of attention to dynamic social and nonsocial stimuli longitudinally in macaques (Macaca mulatta) at 1, 3, and 5 months of age (N = 75) and humans at 2, 4, 6, 8, and 13 months of age (N = 69) using eye tracking. All infants viewed concurrently played silent videos—one social video and one nonsocial video. Both macaque and human infants were faster to look to the social than the nonsocial stimulus, and both species grew faster to orient to the social stimulus with age. Further, macaque infants’ social attention increased linearly from 1 to 5 months. In contrast, human infants displayed a nonlinear pattern of social interest, with initially greater attention to the social stimulus, followed by a period of greater interest in the nonsocial stimulus, and then a rise in social interest from 6 to 13 months. Overall, human infants looked longer than macaque infants, suggesting humans have more sustained attention in the first year of life. These findings highlight potential species similarities and differences, and reflect a first step in establishing baseline patterns of early social attention development.

Attention, Perception, & Psychophysics, 2020

Humans demonstrate enhanced processing of human faces compared with animal faces, known as own-sp... more Humans demonstrate enhanced processing of human faces compared with animal faces, known as own-species bias. This bias is important for identifying people who may cause harm, as well as for recognizing friends and kin. However, growing evidence also indicates a more general face bias. Faces have high evolutionary importance beyond conspecific interactions, as they aid in detecting predators and prey. Few studies have explored the interaction of these biases together. In three experiments, we explored processing of human and animal faces, compared with each other and to nonface objects, which allowed us to examine both own-species and broader face biases. We used a dot-probe paradigm to examine human adults’ covert attentional biases for task-irrelevant human faces, animal faces, and objects.We replicated the own-species attentional bias for human faces relative to animal faces. We also found an attentional bias for animal faces relative to objects, consistent with the proposal that faces broadly receive privileged processing. Our findings suggest that humans may be attracted to a broad class of faces. Further, we found that while participants rapidly attended to human faces across all cue display durations, they attended to animal faces only when they had sufficient time to process them. Our findings reveal that the dot-probe paradigm is sensitive for capturing both own-species and more general face biases, and that each has a different attentional signature, possibly reflecting their unique but overlapping evolutionary importance.

Infant Behavior and Development, 2019

In humans, infants respond positively to slow, gentle stroking—processed by C-tactile (CT) nerve ... more In humans, infants respond positively to slow, gentle stroking—processed by C-tactile (CT) nerve fibers—by showing reductions in stress and increases in eye contact, smiling, and positive vocalizations. More frequent maternal touch is linked to greater activity and connectivity strength in social brain regions, and increases children’s attention to and learning of faces. It has been theorized that touch may prime children for social interactions and set them on a path towards healthy social cognitive development. However, less is known about the effects of touch on young infants’ psychological development, especially in the newborn period, a highly sensitive period of transition with rapid growth in sensory and social processing. It remains untested whether newborns can distinguish CT-targeted touch from other types of touch, or whether there are benefits of touch for newborns’ social, emotional, or cognitive development. In the present study, we experimentally investigated the acute effects of touch in newborn monkeys, a common model for human social development. Rhesus macaques (Macaca mulatta), like humans, are highly social, have complex mother-infant interactions with frequent body contact for the first weeks of life, making them an excellent model of infant sociality. Infant monkeys in the present study were reared in a neonatal nursery, enabling control over their early environment, including all caregiver interactions. One-week-old macaque infants (N = 27) participated in three 5-minute counter-balanced caregiver interactions, all with mutual gaze: stroking head and shoulders (CT-targeted touch), stroking palms of hands and soles of feet (Non-CT touch), or no stroking (No-touch). Immediately following the interaction, infants watched social and nonsocial videos and picture arrays including faces and objects, while we tracked their visual attention with remote eye tracking. We found that, during the caregiver interactions, infants behaved differently while being touched compared to the no-touch condition, irrespective of the body part touched. Most notably, in both touch conditions, infants exhibited fewer stress-related behaviors—self-scratching, locomotion, and contact time with a comfort object—compared to when they were not touched. Following CT-targeted touch, infants were faster to orient to the picture arrays compared to the other interaction conditions, suggesting CT-targeted touch may activate or prime infants’ attentional orienting system. In the No-touch condition infants attended longer to the nonsocial compared to the social video, possibly reflecting a baseline preference for nonsocial stimuli. In contrast, in both touch conditions, infants’ looked equally to the social and nonsocial videos, suggesting that touch may influence the types of visual stimuli that hold infants’ attention. Collectively, our results reveal that newborn macaques responded positively to touch, and touch appeared to influence some aspects of their subsequent attention, although we found limited evidence that these effects are mediated by CT fibers. These findings suggest that newborn touch may broadly support infants’ psychological development, and may have early evolutionary roots, shared across primates. This study illustrates the unique insight offered by nonhuman primates for exploring early infant social touch, revealing that touch may positively affect emotional and attentional development as early as the newborn period.

Journal of Experimental Child Psychology, 2019

Humans rapidly locate and recognize human faces, even in complex environments. In the present stu... more Humans rapidly locate and recognize human faces, even in complex environments. In the present study, we explored some of the social and perceptual features of faces that may contribute to this ability. We measured infant and adult attention to complex, heterogeneous image arrays containing human and animal faces. Arrays were upright or inverted 180°, and in color or grayscale. Infants, age 3 to 5 months (n=51) and 10 to 11 months (n=34), viewed 6-item arrays (Experiment 1), while adults (n=120) searched 64-item arrays (Experiment 2). We found that 3- to 5-montholds already displayed strong own-species biases in face detection—in attention capture, attention holding, and overall detection—suggesting a surprisingly early specialization for human face detection. Furthermore, this remarkable ability was robust, evident even when color and orientation were disrupted, and grew stronger with age. Interestingly, infants’ face detection was reduced by low-level manipulations in a species-specific way, negatively impacting only animal face detection, but not affecting human face detection. In contrast, adults’ face detection efficiency was equally reduced by low-level manipulations across species, suggesting potential age differences in own-species face detection. For infants, social relevance (species) may play a more important role than low-level perceptual features, ensuring infants attend to, connect with, and learn from, the people around them. Efficient human face detection in infancy may reflect the uniqueness of own-species faces as a category, perhaps due to their social relevance.

Developmental Cognitive Neuroscience, 2019

Touch is one of the first senses to develop and one of the earliest modalities for infant-caregiv... more Touch is one of the first senses to develop and one of the earliest modalities for infant-caregiver communication. While studies have explored the benefits of infant touch in terms of physical health and growth, the effects of social touch on infant behavior are relatively unexplored. Here, we investigated the influence of neonatal handling on a variety of domains, including memory, novelty seeking, and social interest, in infant monkeys (Macaca mulatta; n = 48) from 2 to 12 weeks of age. Neonates were randomly assigned to receive extra holding, with or without accompanying face-to-face interactions. Extra-handled infants, compared to standard-reared infants, exhibited less stress-related behavior and more locomotion around a novel environment, faster approach of novel objects, better working memory, and less fear towards a novel social partner. In sum, infants who received more tactile stimulation in the neonatal period subsequently demonstrated more advanced motor, social, and cognitive skills-particularly in contexts involving exploration of novelty-in the first three months of life. These data suggest that social touch may support behavioral development, offering promising possibilities for designing future early interventions, particularly for infants who are at heightened risk for social disorders.

Developmental Science, 2019

We (Meltzoff et al., 2018) described how Oostenbroek et al.’s (2016) design likely dampened infan... more We (Meltzoff et al., 2018) described how Oostenbroek et al.’s (2016) design likely dampened infant imitation. In their commentary, Oostenbroek et al. (2018) argue that our points are post hoc. It is important for readers to know that they are not. Our paper restated “best practices” described in published papers. Based on the literature, the design used by Oostenbroek et al. (2016) would be predicted to dampen infant imitation.

First, Oostenbroek et al.’s (2016) test periods were too brief. The stimulus presentation for each type of gesture was too short to ensure that neonates saw the display. The response measurement period did not allow neonates sufficient time to organize a motor response. Meltzoff and Moore (1983a, 1994) introduced experimental
procedures specifically designed to address these issues (also, Simpson, Murray, Paukner, & Ferrari, 2014). Oostenbroek et al. did not capitalize on these procedural advances.

Second, Oostenbroek et al. allowed uncontrolled experimenter–infant interactions during the test session itself. Previous papers on imitation provided analyses of how uncontrolled interactions with the experimenter can introduce “noise” in experiments of facial imitation (Meltzoff & Moore, 1983b, 1994).

Third, Oostenbroek et al. used suboptimal eliciting conditions. Neonates cannot support their own heads; in Oostenbroek et al., infants’ heads were allowed to flop from side-to- side unsupported on the experimenter’s lap while the experimenter gestured with both hands. In addition, papers have listed techniques for maximizing visual attention (controlled lighting, homogeneous background) (Meltzoff & Moore, 1989, 1994). Oostenbroek et al. tested infants on
a couch in the home.

Despite a design that would blunt imitation, our reanalysis of Oostenbroek et al.’s data showed a response pattern that is consistent with the imitation of tongue protrusion (TP). In their commentary, Oostenbroek et al. (2018) now propose limiting analyses to a subset of their original controls. We reanalyzed their data accordingly. Again, the results support early imitation. Their cross-sectional data (Oostenbroek et al., 2016, Table S4) collapsed across age show significantly more infant TP in response to the TP demonstration than to the mean of the six dynamic face controls (mouth, happy, sad, mmm, ee, and click): t(104) = 4.62, p = 0.00001. The results are also significant using a narrower subset of stimuli (mouth, happy, and sad): t(104) = 3.20, p = 0.0018. These results rule out arousal, because the adult TP demonstration was significantly more effective in eliciting infant tongue protrusions than the category of dynamic face controls. Tongue protrusion matching is a robust phenomenon successfully elicited in more than two dozen studies (reviews: Meltzoff & Moore, 1997; Nagy, Pilling, Orvos, & Molnar, 2013; Simpson et al., 2014).

There are more general lessons to be drawn. Psychology is experiencing what some call a “replication crisis.” Those who attempt to reproduce effects have scientific responsibilities, as do original authors. Both can help psychology become a more cumulative science. It is crucial for investigators to label whether or not a study is a direct replication attempt. If it is not a direct replication, procedural alterations and associated limitations should be discussed. It sows confusion to use procedures that are already predicted to dampen effects, without alerting readers. Psychology will be advanced by more stringent standards for reporting and evaluating studies aimed at reproducing published effects.

Infant imitation is a fundamental skill prior to language and contributes to the development of social cognition. On this both Oostenbroek et al. and we agree.

Developmental Science, 2019

In humans, socioeconomic status (SES) has profound outcomes on socio-emotional development and he... more In humans, socioeconomic status (SES) has profound outcomes on socio-emotional development and health. However, while much is known about the consequences of SES, little research has examined the predictors of SES due to the longitudinal nature of such studies. We sought to explore whether interindividual differences in neonatal sociality, temperament, and early social experiences predicted juvenile social status in rhesus monkeys (Macaca mulatta), as a proxy for SES in humans. We performed neonatal imitation tests in infants’ first week of life and emotional reactivity assessments at 2 and 4 weeks of age. We examined whether these traits, as well as the rearing environment in the first 8 months of life (with the mother or with same-aged peers only) and maternal social status predicted juvenile (2–3 years old) social status following the formation of peer social groups at 8 months. We found that infants who exhibited higher rates of neonatal imitation and newborn emotional reactivity achieved higher social status as juveniles, as did infants who were reared with their mothers, compared to infants reared with peers. Maternal social status was only associated with juvenile status for infant dyads reared in the same maternal group, indicating that relative social relationships were transferred through social experience. These results suggest that neonatal imitation and emotional reactivity may reflect
ingrained predispositions toward sociality that predict later outcomes, and that nonnormative social experiences can alter socio-developmental trajectories. Our results indicate that neonatal characteristics and early social experiences predict later social outcomes in adolescence, including gradients of social stratification.

Developmental Psychobiology, 2019

From birth, human and nonhuman primates attend more to faces with direct gaze compared with avert... more From birth, human and nonhuman primates attend more to faces with direct gaze compared with averted gaze, and previous studies report that attention to the eyes is linked to the emergence of later social skills. Here, we explored whether early experiences influence attraction to eye contact in infant macaques by examining their
attention to face pairs varying in their gaze direction across the first 13 weeks of life. Infants raised by human caretakers had limited conspecific interactions (nurseryreared; N = 16) and were compared to infants raised in rich social environments (mother‐reared; N = 20). Both groups looked longer to faces and the eyes of direct compared to averted‐gaze faces. Looking to all faces and eyes also increased with age. Nursery‐reared infants did not display age‐associated increases in attention to direct‐gaze faces specifically, suggesting that, while there may be an initial preference for direct‐gaze faces from birth, social experiences may support its early development.

Developmental Science, 2018

The meaning, mechanism, and function of imitation in early infancy have been actively discussed s... more The meaning, mechanism, and function of imitation in early infancy have been actively discussed since Meltzoff and Moore's (1977) report of facial and manual imitation by human neonates. Oostenbroek et al. (2016) claim to challenge the existence of early imitation and to counter all interpretations so far offered. Such claims, if true, would have implications for theories of social-cognitive development. Here we identify 11 flaws in Oostenbroek et al.'s experimental design that biased the results toward null effects. We requested and obtained the authors' raw data. Contrary to the authors' conclusions, new analyses reveal significant tongue-protrusion imitation at all four ages tested (1, 3, 6, and 9 weeks old). We explain how the authors missed this pattern and offer five recommendations for designing future experiments. Infant imitation raises fundamental issues about action representation, social learning, and brain–be-havior relations. The debate about the origins and development of imitation reflects its importance to theories of developmental science.

Developmental Cognitive Neuroscience, 2018

Previous developmental research suggests that motor experience supports the development of action... more Previous developmental research suggests that motor experience supports the development of action perception across the lifespan. However, it is still unknown when the neural mechanisms underlying action-perception coupling emerge in infancy. The goal of this study was to examine the neural correlates of action perception during the emergence of grasping abilities in newborn rhesus macaques. Neural activity, recorded via electro-encephalogram (EEG), while monkeys observed grasping actions, mimed actions and means-end movements during the first (W1) and second week (W2) of life was measured. Event-related desynchronization (ERD) during action observation was computed from the EEG in the alpha and beta bands, two components of the sensor-imotor mu rhythm associated with activity of the mirror neuron system (MNS). Results revealed age-related changes in the beta band, but not the alpha band, over anterior electrodes, with greater desynchronization at W2 than W1 for the observation of grasping actions. Additionally, desynchronization to observed grasping actions at W2 was associated with infants' motor skills-measured by a separate behavioral task-such that more grasping attempts were associated to greater beta ERD. These findings suggest the emergence of an early action-perception system, that relies on motor experience, shortly after birth.

Proceedings of the National Academy of Sciences, 2018

Adaptations to stress can occur through epigenetic processes and may be a conduit for informing o... more Adaptations to stress can occur through epigenetic processes and may be a conduit for informing offspring of environmental challenge. We employed ChIP-sequencing for H3K4me3 to examine effects of early maternal deprivation (peer-rearing, PR) in archived rhesus macaque hippocampal samples (male, n = 13). Focusing on genes with roles in stress response and behavior, we assessed the effects of rearing on H3K4me3 binding by ANOVA. We found decreased H3K4me3 binding at genes critical to behavioral stress response , the most robust being the oxytocin receptor gene OXTR, for which we observed a corresponding decrease in RNA expression. Based on this finding, we performed behavioral analyses to determine whether a gain-of-function nonsynonymous OXTR SNP interacted with early stress to influence relevant behavioral stress reactivity phenotypes (n = 194), revealing that this SNP partially rescued the PR phenotype. PR infants exhibited higher levels of separation anxiety and arousal in response to social separation, but infants carrying the alternative OXTR allele did not exhibit as great a separation response. These data indicate that the oxytocin system is involved in social-separation response and suggest that epigenetic down-modulation of OXTR could contribute to behavior-al differences observed in PR animals. Epigenetic changes at OXTR may represent predictive adaptive responses that could impart readiness to respond to environmental challenge or maintain proximity to a caregiver but also contribute to behavioral pathology. Our data also demonstrate that OXTR polymorphism can permit animals to partially overcome the detrimental effects of early maternal deprivation, which could have translational implications for human psychiatric disorders. primate | epigenetic | stress | maternal care | oxytocin S tress is a universal condition of life, but if it is chronic, severe, or occurs during critical developmental windows, it contributes to a variety of disease vulnerabilities, particularly disorders of the brain (1-3). In humans, there are known links between prenatal or early stress and a variety of psychiatric and developmental disorders , including depression, schizophrenia, autism spectrum disorders , posttraumatic stress disorder, anxiety disorders, and substance use disorders (4-6). A major advantage in using animal models is the ability to follow animals prospectively from or before birth and then to control environmental exposure. As such, studies aimed at determining the mechanisms through which in utero or postnatal environments induce long-lasting differences in neurophysiology and behavior have been performed using animal models. Early infant development is a time of high brain plasticity as well as intense mother-infant interaction. For an infant, the mother's behaviors and other cues (i.e., hormones in the milk, pheromones are among the main sources of information about the environment to which an infant must adapt. An early period of enhanced environmental sensitivity has been documented in wild, laboratory, and domestic animals alike. In 1937, the ethologist Lorenz (7) defined a "critical period" for the social bonding that occurs during early development. Bateson later modified the nomenclature, instead referring to a "sensitive period ," which he described as a developmental phase during which events are particularly likely to produce prolonged effects on an individual (8). Years later, rodent studies performed by Levine showed that early experience, as determined by the extent and quality of maternal care, produced long-lasting alterations in hypotha-lamic-pituitary-adrenal (HPA) axis activity, fearfulness, and social behaviors (9). These studies were rapidly replicated and expanded, demonstrating that epigenetic factors played a significant role, especially in stress-sensitive regions of brain such as Significance Epigenetically programmed stress adaptation may be a conduit for informing offspring of environmental challenge. We employed ChIP-sequencing to examine effects of early environment on epigenetic regulation using hippocampal samples from macaques exposed to disruption in maternal care. We found decreased H3K4me3 binding at genes critical to behavioral stress response, the most robust being the oxytocin receptor gene (OXTR), for which we observed a corresponding decrease in RNA expression. Post hoc analysis showed that a gain-of-function OXTR SNP rescued behavioral differences in early stress-exposed subjects. Our data suggest that epigenetic down-modulation of OXTR in brain could contribute to behavioral differences observed in early stress-exposed subjects and that functional genetic variation plays a role. These could have translational implications for human psychiatric disease and personality disorders.

PLOSE ONE, 2017

Neonatal imitation is the matching of (often facial) gestures by newborn infants. Some studies su... more Neonatal imitation is the matching of (often facial) gestures by newborn infants. Some studies suggest that performance of facial gestures is due to general arousal, which may produce false positives on neonatal imitation assessments. Here we examine whether arousal is linked to facial gesturing in newborn infant rhesus macaques (Macaca mulatta). We tested 163 infants in a neonatal imitation paradigm in their first postnatal week and analyzed their lipsmacking gestures (a rapid opening and closing of the mouth), tongue protrusion gestures , and yawn responses (a measure of arousal). Arousal increased during dynamic stimulus presentation compared to the static baseline across all conditions, and arousal was higher in the facial gestures conditions than the nonsocial control condition. However, even after controlling for arousal, we found a condition-specific increase in facial gestures in infants who matched lipsmacking and tongue protrusion gestures. Thus, we found no support for the arousal hypothesis. Consistent with reports in human newborns, imitators' propensity to match facial gestures is based on abilities that go beyond mere arousal. We discuss optimal testing conditions to minimize potentially confounding effects of arousal on measurements of neonatal imitation.

Both human and nonhuman primate adults use infant-directed facial and vocal expressions across ma... more Both human and nonhuman primate adults use infant-directed facial and vocal expressions across many contexts when interacting with infants (e.g., feeding, playing). This infant-oriented style of communication, known as infant-directed speech (IDS), seems to benefit human infants in numerous ways, including facilitating language acquisition. Given the variety of contexts in which adults use IDS, we hypothesized that IDS supports learning beyond the linguistic domain and that these benefits may extend to nonhuman primates. We exposed 2.5-month-old rhesus macaque infants (N = 15) to IDS, adult-directed speech (ADS), and a non-social control (CTR) during a video presentation of unrelated stimuli. After a 5-or 60-minute delay, infants were shown the familiar video side-by- side with a novel video. Infants exhibited a novelty preference after the 5-minute delay, but not after the 60-minute delay, in the ADS and CTR conditions, and a novelty preference in the IDS condition only after the 60-minute delay. These results are the first to suggest that exposure to IDS affects infants’ long-term memory, even in non-linguistic animals.

Human adults and infants show a preference for average faces, which could stem from a general pro... more Human adults and infants show a preference for average faces, which could stem from a general processing mechanism and may be shared among primates. However, little is known about preference for facial averageness in monkeys. We used a comparative developmental approach and eye-tracking methodology to assess visual attention in human and macaque infants to faces naturally varying in their distance from a prototypical face. In Experiment 1, we examined the preference for faces relatively close to or far from the prototype in 12-month-old human infants with human adult female faces. Infants preferred faces closer to the average than faces farther from it. In Experiment 2, we measured the looking time of 3-month-old rhesus macaques (Macaca mulatta) viewing macaque faces varying in their distance from the prototype. Like human infants, macaque infants looked longer to faces closer to the average. In Experiments 3 and 4, both species were presented with unfamiliar categories of faces (i.e., macaque infants tested with adult macaque faces; human infants and adults tested with infant macaque faces) and showed no prototype preferences, suggesting that the prototypicality effect is experience-dependent. Overall, the findings suggest a common processing mechanism across species, leading to averageness preferences in primates.

Behavior Research Methods, 2023

Autism Research, 2020

Japanese Psychological Review, 2019

PLOS ONE, 2019

Developmental Science, 2020

Advances in Methods and Practices in Psychological Science, 2020

Developmental Psychobiology, 2020

Attention, Perception, & Psychophysics, 2020

Infant Behavior and Development, 2019

Journal of Experimental Child Psychology, 2019

Developmental Cognitive Neuroscience, 2019

Developmental Science, 2019

Infant imitation is a fundamental skill prior to language and contributes to the development of social cognition. On this both Oostenbroek et al. and we agree.

Developmental Science, 2019

Developmental Psychobiology, 2019

Developmental Science, 2018

Developmental Cognitive Neuroscience, 2018

Proceedings of the National Academy of Sciences, 2018

PLOSE ONE, 2017

Research mentors strive to ensure that undergraduates gain research skills and develop profession... more Research mentors strive to ensure that undergraduates gain research skills and develop professionally during mentored research experiences in the sciences. We created the SURE (Specialized Undergraduate Research Experience) Workbook, a freely-available, interactive guide to scaffold student learning during this process. The Workbook: (1) identifies mentees' relevant strengths and areas for improvement, (2) encourages effective long-term goal setting, (3) ensures clear communication to facilitate a positive mentor-mentee working relationship, (4) exposes mentees to all phases of the research process, (5) develops mentees' autonomy for research and related professional experiences, and (6) offers mentors a concrete assessment tool to evaluate student participation and development over the course of the research experience. Hands-on research experiences can be invaluable and transformative in undergraduates' professional development, and we predict that the additional structure and standardization provided by the SURE Workbook will help maximize student learning and performance during such experiences. Thinking ahead, mentees who cultivate positive attitudes about research by using the SURE Workbook may be more inclined to pursue research professions and effectively mentor others when they graduate.

Student Notebook, APS Observer, 2011

As graduate students, we are indoctrinated to value those three little words: research, teaching,... more As graduate students, we are indoctrinated to value those three little words: research, teaching, and service. Not the words you had in mind? Welcome to graduate school. Though most of us get a plethora of research experience and numerous opportunities for service, teaching experiences may not be as easily accessible. Given that most jobs in academia require undergraduate teaching, developing the knowledge, resources, and skills to carry out this job are particularly important for graduate students. Teaching experience can give you insight into whether you really want a teaching-focused career. Gaining experiences in teaching throughout your graduate career will aid in the transition to becoming a faculty member. Perhaps most importantly, being able to demonstrate your teaching abilities will make you a more marketable candidate for a job in academia. We offer some tips and resources to get you started.

International Journal of Teaching and Learning in Higher Education, 2012

Google Docs, an online word processing application, is a promising tool for collaborative learnin... more Google Docs, an online word processing application, is a promising tool for collaborative learning. However, many college instructors and students lack knowledge to effectively use Google Docs to enhance teaching and learning. Goals of this study include (1) assessing the effectiveness of using Google Docs in an out-of-class collaborative writing activity through measuring the assignment's influence on students' learning experiences, (2) teaching students to work collaboratively, and (3) teaching students to successfully communicate their understanding and application of concepts through writing. Undergraduate students (N = 35) were randomly assigned to small groups to complete two out-of-class assignments. We compared students' collaborative performance and learning across two assignments, one with Google Docs and one without. We found (1) most students were unfamiliar with Google Docs prior to the study, (2) Google Docs changed the means of communication used in collaborative writing, (3) 93% of students considered Google Docs a useful tool for group work, (4) using Google Docs had no effect on students' paper grades, and (5) half of the students reported they would like to use Google Docs in the future. Our results suggest that Google Docs was a useful tool for collaborative writing and influenced student learning.

Mirror neurons are a type of cell in the nervous system that fires during the production of a goa... more Mirror neurons are a type of cell in the nervous system that fires during the production of a goal directed action or expression and during the observation of that same action or expression.

In this chapter, we highlight the benefits of a comparative developmental approach, not only for ... more In this chapter, we highlight the benefits of a comparative developmental approach, not only for revealing which social cognitive capacities are unique or shared across species, but also for uncovering environmental influences and physiological underpinnings of social understanding in infancy. We discuss human and nonhuman primate infants’ (a) recognition of, and selective attention toward, social agents, (b) affiliation toward conspecifics and similar others, and (c) basic action understanding, as three examples of important social cognitive skills. These skills appear foundational, emerging early in development, and are shared across species, suggesting they may be (some of) the precursors upon which later, higher-order social cognitive abilities are built. Throughout, we emphasize how comparative studies can reveal nuances not readily observable in humans alone, including their developmental stability or plastic, early environmental contributions that may support or hinder such skills, and their underlying neural and physiological mechanisms.

New Frontiers in Mirror Neuron Research (Book), 2015

A developmental approach is critical to understanding mirror neurons and debates surrounding thei... more A developmental approach is critical to understanding mirror neurons and debates surrounding their properties, plasticity, function, and evolution. The presence of inter--individual differences in early social competencies, such as neonatal imitation, are indicative of the complex nature of interactions among genetic, epigenetic, and non--genetic (environmental) factors in shaping action--perception brain networks. In the present review, we propose that three aspects of early social development may explain variability in neonatal imitation, specifically (1) individual differences in sensory--motor matching skills, underpinned by mirror neurons, functioning from birth and refined through postnatal experiences, (2) individual differences in social engagements, with some infants demonstrating stronger preferences for social interactions than others, and (3) more general temperamental differences, such as differences in extroversion or reactivity. We present findings and propose future directions aimed at testing these possibilities by examining individual differences related to imitative skill. Neonatal imitation is a useful tool for assessing infants' sensory--motor matching maturity, social motivation, and temperament, particularly when used with a mindfulness of infants' changing social motivations and expectations. The presence of an action--perception mechanism at birth can be better understood by considering the complex interactions among infants' social competences, sensory--motor skills, environmental influences, and individual differences in social interest and temperament.

Mentoring plays a crucial role in the academic, professional, and personal development of graduat... more Mentoring plays a crucial role in the academic, professional, and personal development of
graduate students, both in the context of scholarly research and teaching. In this chapter, we
discuss the role of mentoring in supporting the teaching-related training of graduate students. Particular attention is given to the unique benefits and challenges that accompany peer mentoring, which involves graduate students working together to improve each other’s teaching skills. In the sections that follow, we describe several examples of peer mentoring and discuss research on peer mentoring’s effects on teacher training. We then identify potential challenges and barriers that can affect the success of peer-mentoring programs. Finally, we highlight some practical considerations related to implementing peer mentoring programs to complement existing teaching assistant (TA) training activities.

The expression of emotions plays a key role in human communication. Besides language, humans use ... more The expression of emotions plays a key role in human communication. Besides language, humans use nonverbal cues such as facial and vocal expressions to convey emotions. The voice is especially important as an emotional medium because it is a carrier for spoken language production. Additionally, listeners can perceive vocal expressions across long distances and in situations where facial or gestural information is not available (e.g., telephone). It is commonly believed that women are better than men in recognizing emotional tone of voice and this belief has been confirmed in behavioral studies. Unfortunately, it is not until recently that sex has been considered as a modulating factor of the brain mechanisms underlying vocal emotion comprehension. Here we present work that sheds some light on the neuroanatomical and temporal underpinnings of these mechanisms as they occur in men and women. Respective findings not only enhance our understanding of vocal emotional comprehension, they also make it clear that research on sex differences in emotion recognition provides useful insight into sex specific interaction patterns that may help explain some of the difficulties that arise when men and women communicate.

Empirical studies are incompatible with the proposal that neonatal imitation is arousal-driven or... more Empirical studies are incompatible with the proposal that neonatal imitation is arousal-driven or declining with age. Nonhuman primate (NHP) studies reveal a functioning brain mirror system from birth, developmental continuity in imitation and later sociability, and the malleability of neonatal imitation, shaped by the early environment. A narrow focus on arousal effects and reflexes may grossly underestimate neonatal capacities.

Behavioral and Brain Sciences

Neonatal imitation should not exclusively be considered at the population-level; instead, we prop... more Neonatal imitation should not exclusively be considered at the population-level; instead, we propose that inconsistent findings regarding its occurrence result from important individual differences in imitative responses. We also highlight what we consider to be a false dichotomy of genetic versus learning accounts of the development of mirror neurons (MNs) and, instead, suggest a more parsimonious epigenetic perspective.

Behavioral and Brain Sciences, 2013

Based on mirror neurons' properties, viewers are emotionally engaged when observing others – even... more Based on mirror neurons' properties, viewers are emotionally engaged when observing others – even when not actively interacting; therefore, characterizing non-participatory action-viewing as isolated may be misleading. Instead, we propose a continuum of socio-emotional engagement. We also highlight recent developmental work that uses a second-person perspective, investigating behavioral, physiological, and neural activity during caregiver–infant interactions.

Behavioral and Brain Sciences, 2010

Gender differences in face-based emotion recognition, notably differential use of mimicry, may co... more Gender differences in face-based emotion recognition, notably differential use of mimicry, may compromise the extent to which the Simulation of Smiles model can be generalized to populations besides the adult females on which it has been tested. Much work indicates sex differences in face-based emotion recognition, including smile recognition.

Behavioral and Brain Sciences, 2008

We present evidence from neuroimaging and brain lesion studies that emotional contagion may not ... more We present evidence from neuroimaging and brain lesion studies
that emotional contagion may not be a mechanism underlying musical emotions. Our brains distinguish voice from non-voice sounds early in processing, and dedicate more resources to such processing. We argue that super-expressive voice theory currently cannot account for evidence of the dissociation in processing musical emotion and voice prosody.