Focus: The Science of Stress: Social Fear in US Infants: The Roles of Hair and Salivary Cortisol

Elevated social fear in infancy poses risk for later social maladjustment and psychopathology. Hair cortisol concentration (HCC), an index of cumulative cortisol exposure, and diurnal salivary cortisol slope, a biomarker of acute stress regulation, have been associated with social fear behaviors in childhood; however, no research has addressed their relations in infancy. Elucidating potential biomarkers of infant social fear behaviors, as well as environmental factors associated with these biomarkers, may grant insights into the ontogeny of fear behaviors that increase risk for internalizing and externalizing psychopathologies later in life. The current study used multiple linear regression to examine if infant HCC, infant diurnal cortisol slope, and income-to-needs ratios (ITN) were differentially associated with observed social fear responses to a Stranger Approach task at 12 months. Using a sample of 90 infants (M_age = 12.26m, SD = 0.81m, 50% female), results indicated that increased infant HCC was associated with increased distress vocalizations during the Stranger Approach task, while steeper diurnal cortisol slope was associated with fewer distress vocalizations. Ordinary least squares path analyses did not reveal group differences between economically strained and non-strained infants in how cortisol measures and social fear responses related. Findings underscore very early psychobiological correlates of fearfulness that may increase risk for fear-related disorders and adverse mental health symptomology across childhood.     

Serotonin transporter gene variation, infant abuse, and responsiveness to stress in rhesus macaque mothers and infants

A functional polymorphism in the promoter region of the serotonin transporter (5-HTTLPR) gene has been associated with variation in anxiety and hypothalamus-pituitary-adrenal (HPA) axis function in humans and rhesus macaques. Individuals carrying the short allele are at a higher risk for developmental psychopathology, and this risk is magnified in short allele carriers who have experienced early life stress. This study investigated the relationship between 5-HTTLPR allelic variation, infant abuse, and behavioral and hormonal responses to stress in rhesus macaques. Subjects were 10 abusive mothers and their infants, and 10 nonabusive mother-infant pairs. Mothers and infants were genotyped for the rh5-HTTLPR, and studied in the first 6 months of infant life. For mothers and infants, we measured social group behavior, behavioral responses to handling procedures, and plasma concentrations of ACTH and cortisol under basal conditions and in response to stress tests. The proportion of individuals carrying the short rh5-HTTLPR allele was significantly higher among abusive mothers than controls. Among mothers and infants, the short allele was associated with higher basal cortisol levels and greater hormonal stress responses in the infants. In addition, infants who carried the short rh5-HTTLPR allele had higher anxiety scores than infants homozygous for the long allele. The rh5-HTTLPR genotype also interacted with early adverse experience to impact HPA axis function in the infants. These results are consistent with those of previous studies which demonstrate associations between serotonergic activity and anxiety and stress reactivity, and add additional evidence suggesting that genetic variation in serotonergic function may contribute to the occurrence of abusive parenting in rhesus macaques and modulate emotional behavior and HPA axis function.     

Rule-governed versus contingency-governed behavior in a self-control task: effects of changes in contingencies

Rule-governed behavior is typically acquired faster than contingency-governed behavior but is less sensitive than contingency-governed behavior to unverbalized contingency changes. The present study investigated these relationships in a computer task frequently used to study human self-control. Instructions for one group of participants contained a hint about how to maximize long-term reinforcement; the other group performed the task without the hint. Participants given the hint came closer to maximizing reinforcement in the long term, but their behavior was less sensitive to an unsignaled contingency change than that of those not given the hint. The study shows that, like other complex behaviors, self-control may be contingency-governed or rule-governed.     

Biodesensitization: Biofeedback-controlled systematic desensitization of the stress response to infant crying

Infant crying can be a source of parental stress both psychologically and physiologically and also may be an antecedent to physical child abuse or neglect. Biodesensitization is a new therapeutic technique that allows people to control the source of stress and develop self-control over their physiological responses to the stress-eliciting stimuli. Randomly assigned between three groups, 15 female participants were either given EEG biofeedback pretraining without stress, pretraining while listening to infant crying, or no stress management pretraining while listening to crying. After the pretraining manipulation all participants had biodesensitization training while listening to infant crying. Compared to control participants who were habituated to crying, stress management training significantly reduced the EEG cortical arousal as well as perceived arousal, and anxiety associated with listening to infant crying. The shift in participants' EEG power spectrum produced by infant crying was significantly correlated with perceived arousal and this relationship was strengthened after biofeedback training. In conjunction with other research, the experimental results suggest that stress management training may help ameliorate an aversive response to infant crying and possibly prevent child abuse as a response to physiological hyperreactivity.The author is grateful to Stan Sadava, Shoshana Tyson, and Joanna Manning for their helpful comments on this paper.     

The early crying paradox

In contemporary Western societies, infants in the first 3 months cry more than at any other time during their life. Although this crying is believed to function to assure nutrition, protection, and mother-infant interaction thought to be essential for later attachment, it also predisposes to complaints of excessive crying (“colic”), discontinuing breast-feeding, and, in the extreme case, child abuse. A resolution of this apparent paradox is proposed based on evidence that elements of caregiving are important determinants of some aspects of early crying. It is argued that early human crying under caretaking conditions typical in Western societies is characterized by prolonged crying bouts, that it is specifically the length of crying bouts (rather than frequency or pattern) that is affected by caregiving practice, and that prolonged crying bouts are probably not characteristic with caretaking practices typical in non-Western societies and possibly in our evolutionary past. It is suggested that caregiving behaviors may recruit normal physiological functions that potentiate cry bout duration in Western caregiving contexts, but reduce it in others. Frequent, short bouts are sufficient, and probably better suited than long bouts, to promote all the positive and presumably adaptive functions claimed for infant crying. Furthermore, they may have provided a mechanism by which infants could enhance their own fitness.     

Birth Timing and Behavioral Responsiveness Predict Individual Differences in the Mother–Infant Relationship and Infant Behavior During Weaning and Maternal Breeding

There is a great deal of variability in mother–infant interactions and infant behavior across the first year of life in rhesus monkeys. The current article has two specific aims: (1) to determine if birth timing predicts variability in the mother–infant relationship and infant behavior during weaning and maternal breeding, and (2) to identify predictors of infant behavior during a period of acute challenge, maternal breeding. Forty‐one mother–infant pairs were observed during weaning when infants were 4.5 months old, and 33 were followed through maternal breeding. Subjective ratings of 16 adjectives reflecting qualities of maternal attitude, mother–infant interactions, and infant attitude were factor analyzed to construct factors relating to the mother–infant relationship (Relaxed and Aggressive) and infant behavior (Positive Engagement and Distress). During weaning, late born infants were more Positively Engaged than peak born infants (ANOVA, P < 0.05); however, birth timing did not affect the mother–infant relationship factors Relaxed and Aggressive or the infant attitude factor Distress. During maternal breeding, early born infants had less Relaxed relationships with their mothers than peak or late born infants, higher Positive Engagement scores than peak or late born infants, and tended to have higher Distress scores than peak born infants (repeated‐measures ANOVA, P < 0.05). In addition, Distress scores were higher during maternal breeding than during the pre‐ and postbreeding phases. Finally, multiple regression (P < 0.05) indicated that while infant behavioral responsiveness predicted infant Positive Engagement during the acute challenge of maternal breeding, qualities of the mother–infant relationship predicted infant Distress. These data suggest that birth timing influences the patterns of mother–infant interactions during weaning and maternal breeding. Additionally, infant behavioral responsiveness and mother–infant relationship quality impact infant social engagement and affect expression, respectively. Am. J. Primatol. 74:734‐746, 2012. © 2012 Wiley Periodicals, Inc.     

Worrying affects associative fear learning: a startle fear conditioning study

A valuable experimental model for the pathogenesis of anxiety disorders is that they originate from a learned association between an intrinsically non-aversive event (Conditioned Stimulus, CS) and an anticipated disaster (Unconditioned Stimulus, UCS). Most anxiety disorders, however, do not evolve from a traumatic experience. Insights from neuroscience show that memory can be modified post-learning, which may elucidate how pathological fear can develop after relatively mild aversive events. Worrying--a process frequently observed in anxiety disorders--is a potential candidate to strengthen the formation of fear memory after learning. Here we tested in a discriminative fear conditioning procedure whether worry strengthens associative fear memory. Participants were randomly assigned to either a Worry (n = 23) or Control condition (n = 25). After fear acquisition, the participants in the Worry condition processed six worrisome questions regarding the personal aversive consequences of an electric stimulus (UCS), whereas the Control condition received difficult but neutral questions. Subsequently, extinction, reinstatement and re-extinction of fear were tested. Conditioned responding was measured by fear-potentiated startle (FPS), skin conductance (SCR) and UCS expectancy ratings. Our main results demonstrate that worrying resulted in increased fear responses (FPS) to both the feared stimulus (CS(+)) and the originally safe stimulus (CS(-)), whereas FPS remained unchanged in the Control condition. In addition, worrying impaired both extinction and re-extinction learning of UCS expectancy. The implication of our findings is that they show how worry may contribute to the development of anxiety disorders by affecting associative fear learning.     

Remembering the Object You Fear: Brain Potentials during Recognition of Spiders in Spider-Fearful Individuals

In the present study we investigated long-term memory for unpleasant, neutral and spider pictures in 15 spider-fearful and 15 non-fearful control individuals using behavioral and electrophysiological measures. During the initial (incidental) encoding, pictures were passively viewed in three separate blocks and were subsequently rated for valence and arousal. A recognition memory task was performed one week later in which old and new unpleasant, neutral and spider pictures were presented. Replicating previous results, we found enhanced memory performance and higher confidence ratings for unpleasant when compared to neutral materials in both animal fearful individuals and controls. When compared to controls high animal fearful individuals also showed a tendency towards better memory accuracy and significantly higher confidence during recognition of spider pictures, suggesting that memory of objects prompting specific fear is also facilitated in fearful individuals. In line, spider-fearful but not control participants responded with larger ERP positivity for correctly recognized old when compared to correctly rejected new spider pictures, thus showing the same effects in the neural signature of emotional memory for feared objects that were already discovered for other emotional materials. The increased fear memory for phobic materials observed in the present study in spider-fearful individuals might result in an enhanced fear response and reinforce negative beliefs aggravating anxiety symptomatology and hindering recovery.     

Eye Movements Index Implicit Memory Expression in Fear Conditioning

The role of contingency awareness in simple associative learning experiments with human participants is currently debated. Since prior work suggests that eye movements can index mnemonic processes that occur without awareness, we used eye tracking to better understand the role of awareness in learning aversive Pavlovian conditioning. A complex real-world scene containing four embedded household items was presented to participants while skin conductance, eye movements, and pupil size were recorded. One item embedded in the scene served as the conditional stimulus (CS). One exemplar of that item (e.g. a white pot) was paired with shock 100 percent of the time (CS+) while a second exemplar (e.g. a gray pot) was never paired with shock (CS-). The remaining items were paired with shock on half of the trials. Participants rated their expectation of receiving a shock during each trial, and these expectancy ratings were used to identify when (i.e. on what trial) each participant became aware of the programmed contingencies. Disproportionate viewing of the CS was found both before and after explicit contingency awareness, and patterns of viewing distinguished the CS+ from the CS-. These observations are consistent with “dual process” models of fear conditioning, as they indicate that learning can be expressed in patterns of viewing prior to explicit contingency awareness.     

Individual and Gender Differences in Subjective and Objective Indices of Pain: Gender,Fear of Pain,Pain Catastrophizing and Cardiovascular Reactivity

According to fear-avoidance models of pain perception, heightened fear of pain may increase disruptive effects of pain; however, the extent to which this affects self-reported pain severity versus physiological indices of pain is not well delineated. The current study examined self-report measures and physiological indices of pain during a cold pressor (CP) task. Individual differences in fear of pain and pain catastrophizing were also assessed via questionnaire. The primary aim of the current study was to examine the extent to which individual differences associated with fear and catastrophizing in response to pain influences subjective and physiological measures of pain. A secondary aim was to examine gender differences associated with response to pain. Average subjective pain ratings were higher for females than males. In contrast, males exhibited higher systolic and diastolic reactivity in response to the CP task relative to females, as well as failure to fully recover to baseline levels. Follow-up correlational analyses revealed that subjective pain ratings were positively associated with fear of pain in both sexes, but were not associated with cardiovascular indices. These results suggest that fear of pain and pain catastrophizing do not influence cardiovascular responses to induced pain. Further research is necessary in order to determine whether these gender differences in blood pressure and heart rate response profiles are due to biological or psychosocial influences. Results support the notion that fear of pain increases subjective pain ratings, but does not influence cardiovascular responses during CP pain-induction.     

Maternal Anxiety in Rhesus Macaques (Macaca mulatta)

Visual monitoring and scratching were used as behavioral indicators of maternal and social anxiety in small captive groups of rhesus macaques. Young infants were especially at risk from other group members during the first weeks of locomotion away from their mothers. Mothers received aggression from other individuals irrespective of their infants' presence or absence. The rate at which mothers scratched themselves increased significantly when their infants moved away from them and when the infants approached or were approached by individuals who frequently harassed them. The rate of maternal scratching and the rate of glancing at the infant and at other individuals when the infant was away decreased as infants grew older and became less vulnerable to harassment. In contrast, the rate of maternal scratching and visual monitoring of other individuals when the infant was in contact remained stable across the first 12 wk of lactation. The rate of maternal scratching increased when the mother-infant pair was in spatial proximity to the adult male or higher ranking adult females. Although visual monitoring and scratching showed a similar sensitivity to social variables, it is speculated that they might reflect different components of anxiety, namely, anticipation of danger and uncertainty due to motivational conflict. The results of this investigation indicate that a macaque mother's emotional reactivity to a perceived danger for herself and her infant can be measured quite accurately using the rates of visual monitoring and scratching and that the latter represent reliable tools to investigate the emotional correlates of maternal behavior in nonhuman primates.     

Disrupting Reconsolidation of Fear Memory in Humans by a Noradrenergic β-Blocker

The basic design used in our human fear-conditioning studies on disrupting reconsolidation includes testing over different phases across three consecutive days. On day 1 - the fear acquisition phase, healthy participants are exposed to a series of picture presentations. One picture stimulus (CS1+) is repeatedly paired with an aversive electric stimulus (US), resulting in the acquisition of a fear association, whereas another picture stimulus (CS2-) is never followed by an US. On day 2 - the memory reactivation phase, the participants are re-exposed to the conditioned stimulus without the US (CS1-), which typically triggers a conditioned fear response. After the memory reactivation we administer an oral dose of 40 mg of propranolol HCl, a β-adrenergic receptor antagonist that indirectly targets the protein synthesis required for reconsolidation by inhibiting the noradrenaline-stimulated CREB phosphorylation. On day 3 - the test phase, the participants are again exposed to the unreinforced conditioned stimuli (CS1- and CS2-) in order to measure the fear-reducing effect of the manipulation. This retention test is followed by an extinction procedure and the presentation of situational triggers to test for the return of fear. Potentiation of the eye blink startle reflex is measured as an index for conditioned fear responding. Declarative knowledge of the fear association is measured through online US expectancy ratings during each CS presentation. In contrast to extinction learning, disrupting reconsolidation targets the original fear memory thereby preventing the return of fear. Although the clinical applications are still in their infancy, disrupting reconsolidation of fear memory seems to be a promising new technique with the prospect to persistently dampen the expression of fear memory in patients suffering from anxiety disorders and other psychiatric disorders.     

Posttraumatic Stress Disorder (PTSD) Patients Exhibit a Blunted Parasympathetic Response to an Emotional Stressor

Diminished parasympathetic reactivity is a physiological feature of posttraumatic stress disorder (PTSD). The objective of this study was to compare female PTSD patients with non-traumatized healthy women with respect to autonomic cardiovascular regulation during exposure to two stressors. Hospitalized PTSD patients (n = 52) and controls (n = 37) completed standardized laboratory-based stress testing including a mental arithmetic test and a standardized audiotape recording of a crying infant. Controls and PTSD patients both showed a significantly increased heart rate and reduced pre-ejection period from baseline rest to the arithmetic stressor. However, as judged from nonsignificant changes in baroreflex sensitivity, parasympathetic activation caused by the crying infant stressor was blunted in PTSD patients as compared to healthy individuals. Under the crying infant condition, a vagal dominance was observed only in controls, and not in PTSD patients. Our data demonstrate that, in PTSD patients, diminished parasympathetic reactivity is not restricted to trauma-related events but can also be observed in response to a social stimulus such as listening to a crying infant. This finding suggests that the altered vagal reactivity in PTSD patients reflects the physiological consequences of a generally disturbed autonomous response to emotionally relevant stressors.     

Individual Day-to-Day Process of Social Anxiety in Vulnerable College Students

Transitions requiring the creation of new social networks may be challenging for individuals vulnerable to social anxiety, which may hinder successful adjustment. Using person-specific methodology, this study examined social anxiety in vulnerable university freshman away from home during their first semester of college to understand how day-to-day processes of social anxiety influenced future social anxiety and social withdrawal. Participants completed daily measures of four components of social anxiety which were examined as a process during a single day, and as a process affecting social anxiety and social withdrawal the next day. For most individuals, same-day fear of negative evaluation was associated with maladaptive cognitive processes (anticipatory processing and post-event rumination) and influenced social withdrawal behaviors. Across time relations were less robust and varied between participants suggesting the importance of situational factors and individual differences. These findings may have implications for the effectiveness of various intervention strategies.     

Physiological reactivity to infant crying: a behavioral genetic study

In this study, we examined adults' cardiac reactivity to repeated infant cry sounds in a genetically informative design. Three episodes of cry stimuli were presented to a sample of 184 adult twin pairs. Cardiac reactivity increased with each cry episode, indicating that subjects were increasingly sensitized to repeated infant distress signals. Non‐parents showed more cardiac reactivity than parents, and males displayed a larger increase in heart rate (HR) in response to repeated cry sounds than females. Multivariate genetic modeling showed that the genetic component of adults' HR while listening to infant crying was substantial. Genetic factors explained 37–51% of the variance in HR and similar genes influenced HR at baseline and HR reactivity to infant crying. The remaining variance in HR across the cry paradigm was accounted for by unique environmental influences (including measurement error). These results point to genetic and experiential effects on HR reactivity to infant crying that may contribute to the explanation of variance in sensitive and harsh parenting.     

Early behavioral development and temperamental traits in mother- vs peer-reared rhesus monkeys

Behavioral characteristics (“traits”) of 24 mother-reared and 24 nursery/peer-reared rhesus monkey infants were assessed via rating scales from the third through the seventh month of life while housed with their rearing partners, and from months 8–10 after all animals had been placed in novel peer groups. The animals were also tested at 8 months of age on the Bayley Scales of Infant Development adapted for nonhuman primates. During the early period effects noted were primarily developmental. Peer-reared animals were rated as increasingly less cautious and more attentive to the outside environment over time, while mother-reared infants declined in ratings of dependence on their mothers. All animals were rated as increasingly active and excitable, and less fearful, over time. For the period of months 8–10, peer-reared animals showed higher confidence ratings in month 10, and all animals showed a decline in attachment to cagemates. Mother-reared animals showed more hostility to the examiner during Bayley testing, whereas peer-reared animals showed more fear. Sex effects included greater ratings for independence from mothers, greater activity over both the early and later periods, greater excitability, greater attentiveness to the extra-cage environment, less cautiousness, and better performance on one Bayley problem for females.     

Relationship of early infant state measures to behavior over the first year of life in the tufted capuchin monkey (Cebus apella)

Data on activity states were collected from 29 group-housed capuchin monkey (Cebus apella) infants for 3 h each week from birth to 11 weeks of age. The amounts of time spent in sleeping/drowsy, alert–quiet, and alert–active states were measured in these subjects. Videotaped observations of these infants were recorded 3 times/week in the home cage over the first year of life and were scored for a number of social and exploratory behaviors. The extent to which early infant activity state scores predicted later behavior in the home cage was examined. Infant state measures correlated significantly with home cage behavior during months 2–6 in that infants that had been more active in early infancy spent more time alone, with other animals, and in exploration and play and less time with mothers than did quieter infants. Early state measures were less successful in predicting home cage scores beyond 8 months of age, whereas differences in behavior attributable to housing variables became more salient in the latter part of the first year. There was also a negative correlation between mother and infant activity in months 2 and 3, in that more sedentary mothers tended to have more active infants. Am. J. Primatol. 44:43–56, 1998. © 1998 Wiley-Liss, Inc. This article is a U.S. Government work, and, as such, is in the public domain in the United States of America.     

The relation of emotions to placebo responses

The hypothesis put forth is that expectations of treatment effects reduce negative emotions and thereby reduce symptoms, e.g. pain. Negative emotions increase pain, and it is hypothesized that placebos reduce pain by reducing negative emotions, i.e. feelings of nervousness, fear and anxiety. Placebo analgesia has been shown to be mediated via opioid activity, and relaxation increases opioid activity. The placebo acquires its relaxing effect due to verbal information that pain will be reduced, or due to associations between the placebo and the reduction in pain after effective treatment. Thus, the placebo signals that unpleasantness will be less after administration of the placebo. This involves negative reinforcement which is due to activation of a dopaminergic system that has been found to be activated during placebo analgesia and is involved in positive emotions. The nocebo effect of increased pain is, consistent with this model, because of increased fear and anxiety. The new aspect of the presented model is the hypothesis that expectations reduce negative emotions, and that negative reinforcement that involves the dopaminergic reinforcement system should be a contributor to placebo responses.     

Bystanders affect the outcome of mother–infant interactions in rhesus macaques

Animal communication involves the transfer of information between a sender and one or more receivers. However, such interactions do not happen in a social vacuum; third parties are typically present, who can potentially eavesdrop upon or intervene in the interaction. The importance of such bystanders in shaping the outcome of communicative interactions has been widely studied in humans, but has only recently received attention in other animal species. Here, we studied bouts of infant crying among rhesus macaques (Macaca mulatta) in order to investigate how the presence of bystanders may affect the outcome of this signalling interaction between infants and mothers. It was hypothesized that, as crying is acoustically aversive, bystanders may be aggressive to the mother or the infant in order to bring the crying bout to a close. Consequently, it was predicted that mothers should acquiesce more often to crying if in the presence of potentially aggressive animals. In line with this prediction, it was found that mothers gave infants access to the nipple significantly more often when crying occurred in the presence of animals that posed a high risk of aggression towards them. Both mothers and infants tended to receive more aggression from bystanders during crying bouts than outside of this time, although such aggression was extremely rare and was received by less than half of the mothers and infants in the study. Mothers were also found to be significantly more aggressive to their infants while the latter were crying than outside of crying bouts. These results provide new insight into the complex dynamics of mother–offspring conflict, and indicate that bystanders may play an important role in shaping the outcome of signalling interactions between infants and their mothers.     

Emotional Processing of Infants Displays in Eating Disorders

Aim

The aim of this study is to examine emotional processing of infant displays in people with Eating Disorders (EDs).

Background

Social and emotional factors are implicated as causal and maintaining factors in EDs. Difficulties in emotional regulation have been mainly studied in relation to adult interactions, with less interest given to interactions with infants.

Method

A sample of 138 women were recruited, of which 49 suffered from Anorexia Nervosa (AN), 16 from Bulimia Nervosa (BN), and 73 were healthy controls (HCs). Attentional responses to happy and sad infant faces were tested with the visual probe detection task. Emotional identification of, and reactivity to, infant displays were measured using self-report measures. Facial expressions to video clips depicting sad, happy and frustrated infants were also recorded.

Results

No significant differences between groups were observed in the attentional response to infant photographs. However, there was a trend for patients to disengage from happy faces. People with EDs also reported lower positive ratings of happy infant displays and greater subjective negative reactions to sad infants. Finally, patients showed a significantly lower production of facial expressions, especially in response to the happy infant video clip. Insecure attachment was negatively correlated with positive facial expressions displayed in response to the happy infant and positively correlated with the intensity of negative emotions experienced in response to the sad infant video clip.

Conclusion

People with EDs do not have marked abnormalities in their attentional processing of infant emotional faces. However, they do have a reduction in facial affect particularly in response to happy infants. Also, they report greater negative reactions to sadness, and rate positive emotions less intensively than HCs. This pattern of emotional responsivity suggests abnormalities in social reward sensitivity and might indicate new treatment targets.