Temporal Dynamics of the Neural Representation of Social Relationships.

Humans can rapidly encode information from faces to support social judgments and facilitate interactions with others. We can also recall complex knowledge about those individuals, such as their social relationships with others, but the time course of this process has not been examined in detail. This study addressed the temporal dynamics of emerging visual and social relationship information using EEG and representational similarity analysis. Participants (female = 23, male = 10) became familiar with a 10-person social network, and were then shown faces of that network's members while EEG was recorded. To examine the temporal dynamics of the cognitive processes related to face perception, we compared the similarity structure of neural pattern responses to models of visual processing, face shape similarity, person identity, and social relationships. We found that all types of information are associated with neural patterns after a face is seen. Visual models became significant early after image onset, and identity across a change in facial expression was uniquely associated with neural patterns at several points throughout the time course. Additionally, a model reflecting perceived frequency of social interaction was present beginning at ∼110 ms, even in the absence of an explicit task to think about the relationships among the network members. This study highlights the speed and salience of social information relating to group dynamics that are present in the brain during person perception.SIGNIFICANCE STATEMENT We live our lives in social groups where complex relationships form among and around us. It is likely that some of the information about social relationships that we observe is integral during person perception, to better help us interact in differing situations with a variety of people. However, when exactly this information becomes relevant has been unclear. In this study, we present evidence that information reflecting observed relationships among a social network is spontaneously represented in whole-brain patterns shortly following presentation of a face. These results are consistent with neuroimaging studies showing spontaneous spatial representation of social network characteristics, and contribute novel insights into the timing of these neural processes.

Maternal Neurobiological Processing of Negative Adolescent Stimuli: Relations With Positive Parenting and Relationship Quality.

We examined associations between maternal affective neurobiology and positive parenting in a study of 20 mothers of adolescents. Mothers underwent functional magnetic resonance imaging during an emotion image task, rated parent-adolescent relationship quality, and completed an adolescent interaction task in which positive parenting behaviors were observed. Maternal structure was associated with lower responsivity in emotional processing regions in the general negative image contrast and was related to greater dorsolateral prefrontal cortex activation to negative adolescent images. Parent-adolescent relationship quality was associated with lower precuneus activation to negative adolescent images. Findings are among the first to connect functional brain processing with observed parenting behaviors for parents of adolescent children, and underscore the relative importance of affective processing in parenting older children.

The relation between craving and binge eating: Integrating neuroimaging and ecological momentary assessment.

The role of craving in binge eating characteristic of bulimia nervosa (BN) is inconclusive. A network of regions associated with cue reactivity to food and substances has been identified, comprised of the amygdala, orbitofrontal cortex, insula, and striatum. The goal of this study was to examine individual differences in BOLD response in this appetitive network as moderators of the relationship between craving and binging in the natural environment in women with BN. Women with BN (N = 16) completed a baseline measure of craving and a fMRI scan, where they viewed neutral cues and food cues. After each run, craving for food was assessed. Participants then completed an ecological momentary assessment six times a day via smart phone and recorded binge eating and craving. Participants exhibited significantly increased BOLD response in the left amygdala in response to food cues compared to neutral cues. However, individual differences in BOLD response were not correlated with self-report craving throughout the scan. The relationship between craving and binging in everyday life was moderated by individual differences in activation in the caudate, insula, and amygdala. Women with greater activation in these regions demonstrated significant increases in craving prior to binge eating. Those who did not exhibit increases in activation did not exhibit increases in craving prior to binge eating in the natural environment. Craving may not underlie binge eating for all individuals with BN. However, these results indicate that neural response to food cues may affect individual differences in the daily experience of craving and binge eating.

Functional correlates of likelihood and prior representations in a virtual distance task.

Spatial navigation is an imperative cognitive function, in which individuals must interact with their environment in order to accurately reach a destination. Previous research has demonstrated that, when traveling a predetermined distance, humans must balance between noise in the measurement process and the prior history of traveled distances. This tradeoff has recently been formally described using Bayesian estimation; however, the neural correlates of Bayesian estimation during distance reproduction have yet to be investigated. Here, human subjects performed a virtual reality distance reproduction task during functional Magnetic Resonance Imaging (fMRI), in which they were required to reproduce various traveled distances in the absence of overt navigational cues. As previously demonstrated, subjects exhibited a central tendency effect, wherein reproduced distances gravitated to the mean of the stimulus set. fMRI activity during this task revealed distance-sensitive activity in a network of regions, including prefrontal and hippocampal regions. Using a computational index of central tendency, we found that activity in the retrosplenial cortex, a region highly implicated in spatial navigation, negatively covaried between subjects with the degree of central tendency observed; conversely, we found that activity in the anterior hippocampus/amygdala complex was positively correlated with the central tendency effect of gravitating to the average reproduced distance. These findings suggest dissociable roles for the retrosplenial cortex and hippocampal complex during distance reproduction, with both regions coordinating with the prefrontal cortex the influence of prior history of the environment with present experience. Hum Brain Mapp 37:3172-3187, 2016. © 2016 Wiley Periodicals, Inc.

Uncertainty-dependent activity within the ventral striatum predicts task-related changes in response strategy.

Recent neuroimaging work has demonstrated that the ventral striatum (VS) encodes confidence in perceptual decisions. However, it remains unclear whether perceptual uncertainty can signal the need to adapt behavior (such as by responding more cautiously) and whether such behavioral changes are related to uncertainty-dependent activity within the VS. Changes in response strategy have previously been observed following errors and are associated with both medial frontal cortex (MFC) and VS, two components of the performance-monitoring network. If uncertainty can elicit changes in response strategy (slowing), then one might hypothesize that these changes rely on the performance-monitoring network. In the present study, we investigated the link between perceptual uncertainty and task-related behavioral adaptations (response slowing and accuracy increases), as well as how such behavioral changes relate to uncertainty-dependent activity within MFC and VS. Our participants performed a two-choice perceptual decision-making task in which perceptual uncertainty was reported on each trial while behavioral and event-related functional magnetic resonance imaging data were collected. Analysis of the behavioral data revealed that uncertain (but correct) responses led to slowing on subsequent trials, a phenomenon that was positively correlated with increased accuracy. Critically, post-uncertainty slowing was negatively correlated with the VS activity elicited by uncertain responses. In agreement with previous reports, increases in MFC activation were observed for uncertain responses, although MFC activity was not correlated with post-uncertainty slowing. These results suggest that perceptual uncertainty can serve as a signal to adapt one's response strategy and that such behavioral changes are closely tied to the VS, a key node in the performance-monitoring network.

Reprint of "Biological motion perception links diverse facets of theory of mind during middle childhood".

Two cornerstones of social development-social perception and theory of mind-undergo brain and behavioral changes during middle childhood, but the link between these developing domains is unclear. One theoretical perspective argues that these skills represent domain-specific areas of social development, whereas other perspectives suggest that both skills may reflect a more integrated social system. Given recent evidence from adults that these superficially different domains may be related, the current study examined the developmental relation between these social processes in 52 children aged 7 to 12years. Controlling for age and IQ, social perception (perception of biological motion in noise) was significantly correlated with two measures of theory of mind: one in which children made mental state inferences based on photographs of the eye region of the face and another in which children made mental state inferences based on stories. Social perception, however, was not correlated with children's ability to make physical inferences from stories about people. Furthermore, the mental state inference tasks were not correlated with each other, suggesting a role for social perception in linking various facets of theory of mind.

Biological motion perception links diverse facets of theory of mind during middle childhood.

Two cornerstones of social development--social perception and theory of mind--undergo brain and behavioral changes during middle childhood, but the link between these developing domains is unclear. One theoretical perspective argues that these skills represent domain-specific areas of social development, whereas other perspectives suggest that both skills may reflect a more integrated social system. Given recent evidence from adults that these superficially different domains may be related, the current study examined the developmental relation between these social processes in 52 children aged 7 to 12 years. Controlling for age and IQ, social perception (perception of biological motion in noise) was significantly correlated with two measures of theory of mind: one in which children made mental state inferences based on photographs of the eye region of the face and another in which children made mental state inferences based on stories. Social perception, however, was not correlated with children's ability to make physical inferences from stories about people. Furthermore, the mental state inference tasks were not correlated with each other, suggesting a role for social perception in linking various facets of theory of mind.

Repetition enhancement and memory effects for duration.

A remarkable aspect of conscious perception is that moments carryover from one to the next, also known as temporal continuity. This ability is thus crucial for detecting regularities, such as in speech and music, and may rely on an accurate perception of time. Investigations of human time perception have detailed two electroencephalographic (EEG) components associated with timing, the contingent negative variation (CNV) and late positive component of timing (LPCt); however, the precise roles of these components in timing remain elusive. Recently, we demonstrated that the perception of duration is influenced by durations presented on prior trials, which we explained by the creation of an implicit memory standard that adapts to local changes in sequence presentation. Here, we turn to the neural basis of this effect. Human participants performed a temporal bisection task in which they were required to classify the duration of auditory stimuli into short and long duration categories; crucially, the presentation order was first-order counterbalanced, allowing us to measure the effect of each presented duration on the next. EEG recordings revealed that the CNV and LPCt signals both covaried with the duration presented on the current trial, with CNV predicting reaction time and LPCt predicting choice. Additionally, both signals covaried with the duration presented in the prior trial but in different ways, with the CNV amplitude reflecting the change in the memory standard and the LPCt reflecting decision uncertainty. Furthermore, we observed a repetition enhancement effect of duration only for the CNV, suggesting that this signal additionally indexes the similarity of successive durations. These findings demonstrate dissociable roles for the CNV and LPCt, and demonstrate that both signals are continuously updated on a trial-by-trial basis that reflects shifts in temporal decisions.

Neurocognitive enhancement in older adults: comparison of three cognitive training tasks to test a hypothesis of training transfer in brain connectivity.

The ultimate goal of cognitive enhancement as an intervention for age-related cognitive decline is transfer to everyday cognitive functioning. Development of training methods that transfer broadly to untrained cognitive tasks (far transfer) requires understanding of the neural bases of training and far transfer effects. We used cognitive training to test the hypothesis that far transfer is associated with altered attentional control demands mediated by the dorsal attention network and trained sensory cortex. In an exploratory study, we randomly assigned 42 healthy older adults to six weeks of training on Brain Fitness (BF-auditory perception), Space Fortress (SF-visuomotor/working memory), or Rise of Nations (RON-strategic reasoning). Before and after training, cognitive performance, diffusion-derived white matter integrity, and functional connectivity of the superior parietal cortex (SPC) were assessed. We found the strongest effects from BF training, which transferred to everyday problem solving and reasoning and selectively changed integrity of occipito-temporal white matter associated with improvement on untrained everyday problem solving. These results show that cognitive gain from auditory perception training depends on heightened white matter integrity in the ventral attention network. In BF and SF (which also transferred positively), a decrease in functional connectivity between SPC and inferior temporal lobe (ITL) was observed compared to RON-which did not transfer to untrained cognitive function. These findings highlight the importance for cognitive training of top-down control of sensory processing by the dorsal attention network. Altered brain connectivity - observed in the two training tasks that showed far transfer effects - may be a marker for training success.

Social-network complexity in humans is associated with the neural response to social information.

Humans have evolved to thrive in large and complex social groups, and it is likely that this increase in group complexity has come with a greater need to decode and respond to complex and uncertain communicatory signals. In this functional MRI study, we examined whether complexity of social networks in humans is related to the functioning of brain regions key to the perception of basic, nonverbal social stimuli. Greater activation to biological than to scrambled motion in the right posterior superior temporal sulcus (pSTS) and right amygdala were positively correlated with the diversity of social-network roles. In the pSTS, in particular, this association was not due to a relationship between network diversity and network size. These findings suggest that increased functioning of brain regions involved in decoding social signals might facilitate the detection and decoding of subtle signals encountered in varied social settings.

Sex differences in emotion- and reward-related neural responses predicting increases in substance use in adolescence.

Adolescent substance use is a significant public health problem and there is a need for effective substance use preventions. To develop effective preventions, it is important to identify neurobiological risk factors that predict increases in substance use in adolescence and to understand potential sex differences in risk mechanisms. The present study used functional magnetic resonance imaging and hierarchical linear modeling to examine negative emotion- and reward-related neural responses in early adolescence predicting growth in substance use to middle adolescence in 81 youth, by sex. Adolescent neural responses to negative emotional stimuli and monetary reward receipt were assessed at age 12-14. Adolescents reported on substance use at age 12-14 and at 6 month, and 1, 2, and 3 year follow-ups. Adolescent neural responses did not predict initiation of substance use (yes/no), but, among users, neural responses predicted growth in substance use frequency. For girls, heightened right amygdala responses to negative emotional stimuli in early adolescence predicted growth in substance use frequency through middle adolescence. For boys, blunted left nucleus accumbens and bilateral ventromedial prefrontal cortex responses to monetary reward predicted growth in substance use frequency. Findings suggest different emotion and reward-related predictors of the development of substance use for adolescent girls versus boys.

Form and motion make independent contributions to the response to biological motion in occipitotemporal cortex.

Psychophysical and computational studies have provided evidence that both form and motion cues are used in the perception of biological motion. However, neuroimaging and neurophysiological studies have suggested that the neural processing of actions in temporal cortex might rely on form cues alone. Here we examined the contribution of form and motion to the spatial pattern of response to biological motion in ventral and lateral occipitotemporal cortex, using functional magnetic resonance imaging (fMRI) and multivoxel pattern analysis (MVPA). We found that selectivity to intact versus scrambled biological motion in lateral occipitotemporal cortex was correlated with selectivity for bodies and not for motion. However, this appeared to be due to the fact that subtracting scrambled from intact biological motion removes any contribution of local motion cues. Instead, we found that form and motion made independent contributions to the spatial pattern of responses to biological motion in lateral occipitotemporal regions MT, MST, and the extrastriate body area. The motion contribution was position-dependent, and consistent with the representation of contra- and ipsilateral visual fields in MT and MST. In contrast, only form contributed to the response to biological motion in the fusiform body area, with a bias towards central versus peripheral presentation. These results indicate that the pattern of response to biological motion in ventral and lateral occipitotemporal cortex reflects the linear combination of responses to form and motion.

Task-based functional connectivity patterns: Links to adolescent emotion regulation and psychopathology.

Adolescence is a developmental period characterized by heightened emotional reactivity, neurobiological changes, and increased rates of anxiety and depression. Emotion regulation (ER) difficulties-or the inability to effectively regulate one's emotions-have been theoretically and empirically conceptualized as a transdiagnostic factor implicated in virtually all forms of psychopathology among youth. The current fMRI study investigates how young adolescents' ER abilities longitudinally mediate the relationship between their task-based (n=67) limbic-prefrontal functional connectivity values and subsequent levels of internalizing and externalizing symptoms. Findings revealed that adolescents with stronger limbic-prefrontal connectivity when viewing negative emotional images reported more ER difficulties one year later which, in turn, predicted higher levels of adolescent-reported internalizing and externalizing symptoms (with the exception of ADHD) two years later. This is the only study to date that provides compelling-albeit preliminary-evidence that ER problems longitudinally mediate the association between task-based functional connectivity patterns and future psychological symptoms among adolescents. Of note, participants were only scanned at baseline, limiting our ability to assess change in adolescents' task-based functional connectivity patterns as a function of developing ER abilities or burgeoning psychological symptomology. In sum, rather than conferring risk for any particular disorder, our results suggest that functional connectivity and subsequent ER abilities may serve a transdiagnostic risk factor for psychopathology. These findings may inform future emotion-focused prevention and intervention efforts aimed at youth susceptible to future internalizing and externalizing problems.

Behavioral inhibition and approach tendencies are associated with striatal activation to loss: Implications for adolescent substance use.

Behavioral inhibition/avoidance and approach systems (BIS/BAS), which facilitate avoidance of aversive stimuli and approach of enticing stimuli, are thought to underlie engagement in substance use (SU). However, little is known about the neural correlates of these systems, particularly in adolescence. The current study examined associations between BIS/BAS tendencies and neural response to reward and loss and then examined whether there was an indirect effect of BIS/BAS on later SU initiation through these neural responses. 79 12-14 year olds underwent fMRI at baseline during a card guessing task. Adolescents reported on their BIS/BAS at baseline and on their SU at baseline and through a 3-year follow-up period. Results showed that higher BIS was associated with lower striatal activation and higher BAS with higher striatal activation to monetary loss. BIS and BAS were not associated with neural activation to monetary reward. There was no support that BIS or BAS predicted SU initiation through striatal activation to monetary loss. Overall, these results may suggest that adolescents with the tendency to avoid aversive stimuli assign less salience and adolescents with the tendency to approach enticing stimuli assign more salience to monetary loss.

Object-based attentional modulation of biological motion processing: spatiotemporal dynamics using functional magnetic resonance imaging and electroencephalography.

Although it is well documented that the ability to perceive biological motion is mediated by the lateral temporal cortex, whether and when neural activity in this brain region is modulated by attention is unknown. In particular, it is unclear whether the processing of biological motion requires attention or whether such stimuli are processed preattentively. Here, we used functional magnetic resonance imaging, high-density electroencephalography, and cortically constrained source estimation methods to investigate the spatiotemporal effects of attention on the processing of biological motion. Directing attention to tool motion in overlapping movies of biological motion and tool motion suppressed the blood oxygenation level-dependent (BOLD) response of the right superior temporal sulcus (STS)/middle temporal gyrus (MTG), while directing attention to biological motion suppressed the BOLD response of the left inferior temporal sulcus (ITS)/MTG. Similarly, category-based modulation of the cortical current source density estimates from the right STS/MTG and left ITS was observed beginning at approximately 450 ms following stimulus onset. Our results indicate that the cortical processing of biological motion is strongly modulated by attention. These findings argue against preattentive processing of biological motion in the presence of stimuli that compete for attention. Our findings also suggest that the attention-based segregation of motion category-specific responses only emerges relatively late (several hundred milliseconds) in processing.

Neural activation to loss and reward among alcohol naive adolescents who later initiate alcohol use.

Adolescent alcohol use is associated with adverse psychosocial outcomes, including an increased risk of alcohol use disorder in adulthood. It is therefore important to identify risk factors of alcohol initiation in adolescence. Research to date has shown that altered neural activation to reward is associated with alcohol use in adolescence; however, few studies have focused on neural activation to loss and alcohol use. The current study examined neural activation to loss and reward among 64 alcohol naive 12-14 year olds that did (n = 20) and did not initiate alcohol use by a three year follow-up period. Results showed that compared to adolescents that did not initiate alcohol use, adolescents that did initiate alcohol use by the three year follow-up period had increased activation to loss in the left striatum (i.e., putamen), right precuneus, and the brainstem/pons when they were alcohol naive at baseline. By contrast, alcohol initiation was not associated with neural activation to winning a reward. These results suggest that increased activation in brain regions implicated in salience, error detection/self-referential processing, and sensorimotor function, especially to negative outcomes, may represent an initial vulnerability factor for alcohol use in adolescence.

Affective Neural Mechanisms of a Parenting-Focused Mindfulness Intervention.

OBJECTIVES: Behavioral evidence suggests that parenting-focused mindfulness interventions can improve parenting practices and enhance family wellbeing, potentially operating through altered emotional processing in parents. However, the mechanisms through which parent mindfulness interventions achieve their positive benefits have not yet been empirically tested, knowledge which is key to refine and maximize intervention effects. Thus, as part of a randomized controlled trial, the present study examined the affective mechanisms of an 8-week parenting-focused mindfulness intervention, the Parenting Mindfully (PM) intervention, versus a minimal-intervention parent education control. METHODS: Twenty highly stressed mothers of adolescents completed pre- and post-intervention behavioral and fMRI sessions, in which mothers completed a parent-adolescent conflict interaction, fMRI emotion task, and fMRI resting state scan. Mothers reported on their mindful parenting, and maternal emotional reactivity to the parent-adolescent conflict task was assessed via observed emotion expression, self-reported negative emotion, and salivary cortisol reactivity. RESULTS: Results indicated that the PM intervention increased brain responsivity in left posterior insula in response to negative affective stimuli, and altered resting state functional connectivity in regions involved in self-reference, behavioral regulation, and social-emotional processing. Changes in mothers' brain function and connectivity were associated with increased mindful parenting and decreased emotional reactivity to the parent-adolescent conflict task. CONCLUSIONS: Findings suggest that mindfulness-based changes in maternal emotional awareness at the neurobiological level are associated with decreased emotional reactivity in parenting interactions, illuminating potential neurobiological targets for future parent-focused intervention.

The first time ever I saw your face.

The perception of social information is crucial for the survival of most animal species. Two recent studies demonstrate the joint contribution of innate mechanisms and perceptual experience to two aspects of social perception--faces and biological motion. Together, they highlight how important it is to consider faces and biological motion as different visual properties used by a broader social perception system.

The Neural Representational Space of Social Memory.

Social functioning involves learning about the social networks in which we live and interact; knowing not just our friends, but also who is friends with our friends. This study utilized an incidental learning paradigm and representational similarity analysis (RSA), a functional MRI multivariate pattern analysis technique, to examine the relationship between learning social networks and the brain's response to the faces within the networks. We found that accuracy of learning face pair relationships through observation is correlated with neural similarity patterns to those pairs in the left temporoparietal junction (TPJ), the left fusiform gyrus, and the subcallosal ventromedial prefrontal cortex (vmPFC), all areas previously implicated in social cognition. This model was also significant in portions of the cerebellum and thalamus. These results show that the similarity of neural patterns represent how accurately we understand the closeness of any two faces within a network. Our findings indicate that these areas of the brain not only process knowledge and understanding of others, but also support learning relations between individuals in groups.