Juvenile stress potentiates aversive 22-kHz ultrasonic vocalizations and freezing during auditory fear conditioning in adult male rats

Traumatic experiences that occur during adolescence can render individuals vulnerable to mood and anxiety disorders. A model in juvenile rats (age: 27-29 days) was developed previously to study the long-term effects of adolescent stress exposure on behaviour and physiology. This paradigm, termed juvenile stress, involves subjecting juvenile rats to different stressors on consecutive days over a 3-day period. Here, we investigated the effects of the juvenile stress paradigm on freezing behaviour and aversive 22-kHz ultrasonic vocalizations (USVs) during auditory fear conditioning in adult male rats (age: 68-90 days). We found that rats previously subjected to juvenile stress increased aversive 22-kHz USVs (total calls and time spent calling) compared with controls during fear-conditioning training. The acoustic USV parameters between control and juvenile stress rats were largely equivalent, including duration, peak frequency and amplitude. While rats did not differ in freezing behaviour during fear conditioning, juvenile stress rats exhibited greater cue-conditioned freezing upon testing 24 h later. Our results show that juvenile stress elicited different long-term changes in freezing and aversive USVs during fear conditioning. Furthermore, they highlight the importance of assessing USVs to detect experience-dependent differences between control and stress-exposed animals which are not detectable by measuring visible behaviour.     

A comparative study of rodent ultrasonic vocalizations during copulation

The temporal patterning of ultrasonic vocalizations (USVs) during copulation was recorded for male-female pairs of Djungarian hamsters (Phodopus campbelli), prairie voles (Microtus ochrogaster), and montane voles (Microtus montanus). Each species appears to utilize a single major frequency band for USVs, centered around 31 kHz for the vole species and 71 kHz for hamsters. Djungarian hamsters exhibited low rates of USVs prior to introduction of the female and following ejaculation, but a high USV rate during periods of copulatory activity. Both vole species called at high rates during all stages of the copulatory sequence, although calling rates decreased following ejaculation. Anesthetization trials, where one pair member was awake and the other anesthesized, suggest that it is the male of each species that produces most USVs. The results were compared with six other muroid species for which data on the temporal patterning of USVs during copulation are available. These data extend our knowledge of the patterning of USVs during copulatory behavior and suggest the need for additional comparative investigations.     

Asymmetrical stimulus generalization following differential fear conditioning

Rodent ultrasonic vocalizations (USVs) are ethologically critical social signals. Rats emit 22 kHz USVs and 50 kHz USVs, respectively, in conjunction with negative and positive affective states. Little is known about what controls emotional reactivity to these social signals. Using male Sprague–Dawley rats, we examined unconditional and conditional freezing behavior in response to the following auditory stimuli: three 22 kHz USVs, a discontinuous tone whose frequency and on–off pattern matched one of the USVs, a continuous tone with the same or lower frequencies, a 4 kHz discontinuous tone with an on–off pattern matched to one of the USVs, and a 50 kHz USV. There were no differences among these stimuli in terms of the unconditional elicitation of freezing behavior. Thus, the stimuli were equally neutral before conditioning. During differential fear conditioning, one of these stimuli (the CS⁺) always co-terminated with a footshock unconditional stimulus (US) and another stimulus (the CS⁻) was explicitly unpaired with the US. There were no significant differences among these cues in CS⁺-elicited freezing behavior. Thus, the stimuli were equally salient or effective as cues in supporting fear conditioning. When the CS⁺ was a 22 kHz USV or a similar stimulus, rats discriminated based on the principal frequency and/or the temporal pattern of the stimulus. However, when these same stimuli served as the CS⁻, discrimination failed due to generalization from the CS⁺. Thus, the stimuli differed markedly in the specificity of conditioning. This strikingly asymmetrical stimulus generalization is a novel bias in discrimination.     

Touch attenuates infants’ physiological reactivity to stress

Animal studies demonstrate that maternal touch and contact regulate infant stress, and handling during periods of maternal deprivation attenuates the stress response. To measure the effects of touch on infant stress reactivity during simulated maternal deprivation, 53 dyads were tested in two paradigms: still‐face (SF) and still‐face with maternal touch (SF+T). Maternal and infant cortisol levels were sampled at baseline, reactivity, and recovery and mother’s and infant’s cardiac vagal tone were measured during the free play, still‐face, and reunion episodes of the procedure. Cortisol reactivity was higher among infants in the SF condition and while cortisol decreased at recovery for infants in the SF+T, it further increased for those in the SF. Vagal tone showed a greater suppression when SF was not accompanied by maternal touch. Touch synchrony during free play was associated with higher infant vagal tone, whereas touch myssynchrony – maternal tactile stimulation while the infant gaze averts – correlated with higher maternal and infant cortisol. In humans, as in mammals, the provision of touch during moments of maternal unavailability reduces infants’ physiological reactivity to stress.     

Rodent ultrasonic vocalizations as biomarkers of future alcohol use: A predictive analytic approach

Excessive alcohol consumption has a vast, negative impact on society. Rodent models have been successful in furthering our understanding of the biological underpinnings that drive alcohol consumption. Rodents emit ultrasonic vocalizations (USVs) that are each composed of several acoustic characteristics (e.g., frequency, duration, bandwidth, power). USVs reflect neurotransmitter activity in the ascending limb of the mesolimbic dopaminergic and cholinergic neurotransmitter systems and serve as noninvasive, real-time biomarkers of dopaminergic and cholinergic neurotransmission in the limbic system. In the present study, we recorded spontaneously emitted USVs from alcohol-naïve Long-Evans (LE) rats and then measured their alcohol intake. We compared the USV acoustic characteristics and alcohol consumption data from these LE rats with previously published data from selectively bred high-alcohol (P and HAD-1) and low-alcohol (NP and LAD-1) drinking lines from studies with the same experimental method. Predictive analytic techniques were applied simultaneously to this combined data set and revealed that (a) USVs emitted by alcohol-naïve rats accurately discriminated among high-alcohol consuming, LE, and low-alcohol consuming rat lines, and (b) future alcohol consumption in these same rat lines was reliably predicted from the USV data collected in an alcohol-naïve state. To our knowledge, this is the first study to show that alcohol consumption is predicted directly from USV profiles of alcohol-naïve rats. Because USV acoustic characteristics are sensitive to underlying neural activity, these findings suggest that baseline differences in mesolimbic cholinergic and dopaminergic tone could determine the propensity for future alcohol consumption in rodents.     

Mouse vocal communication system: Are ultrasounds learned or innate?

Mouse ultrasonic vocalizations (USVs) are often used as behavioral readouts of internal states, to measure effects of social and pharmacological manipulations, and for behavioral phenotyping of mouse models for neuropsychiatric and neurodegenerative disorders. However, little is known about the neurobiological mechanisms of rodent USV production. Here we discuss the available data to assess whether male mouse song behavior and the supporting brain circuits resemble those of known vocal non-learning or vocal learning species. Recent neurobiology studies have demonstrated that the mouse USV brain system includes motor cortex and striatal regions, and that the vocal motor cortex sends a direct sparse projection to the brainstem vocal motor nucleus ambiguous, a projection previously thought be unique to humans among mammals. Recent behavioral studies have reported opposing conclusions on mouse vocal plasticity, including vocal ontogeny changes in USVs over early development that might not be explained by innate maturation processes, evidence for and against a role for auditory feedback in developing and maintaining normal mouse USVs, and evidence for and against limited vocal imitation of song pitch. To reconcile these findings, we suggest that the trait of vocal learning may not be dichotomous but encompass a broad spectrum of behavioral and neural traits we call the continuum hypothesis, and that mice possess some of the traits associated with a capacity for limited vocal learning.     

The Still-Face Paradigm and bidirectionality: Associations with maternal sensitivity,self-esteem and infant emotional reactivity

The Still-Face Paradigm (SFP) is a structured stressful event within which researchers have investigated the influence of maternal psychological and behavioral characteristics on infant behavior. The present investigation contributes to this body of work by examining the joint contributions of maternal and child behavioral and affective characteristics on subsequent behaviors and affectations following the SFP. A sample of non-clinically depressed mothers and their infants (n = 31) engaged in a modified Still-Face Paradigm (SFP), followed by a period of toy play. These interactions were videotaped and behaviorally coded along the following dimensions: maternal sensitivity prior to the SFP and during toy play, infant negative emotional reactivity during the still-face, and infant resistance during the reunion phase. Additionally, mothers reported global self-esteem and this was examined as a predictor of infant behavior. Results revealed significant bidirectional influences such that maternal self-esteem predicted infant emotional reactivity, maternal sensitivity pre-SFP predicted infant resistance during the reunion phase, and infant resistance predicted subsequent levels of maternal sensitivity. Indirect effects were also examined, and provided additional support for bidirectionality in mother–infant interactions. Implications for clinical practice are discussed in light of these findings.     

Maternal Sensitivity: Evidence of Stability across Time,Contexts, and Measurement Instruments

Although maternal sensitivity is widely understood as having a direct impact on the quality of the mother–child relationship, empirical evidence supporting this has been inconsistent, possibly because of varied definitions of the construct and limitations of measurements. The Maternal Behavior Q‐Set (MBQS) appears to be a promising measure of sensitivity, showing associations with attachment security (r = .60) higher than those reported (r = .24) in a highly‐regarded meta‐analysis of other sensitivity measures. The present study aimed to further establish the validity and utility of the MBQS by exploring its consistency with a contingency‐based measure of sensitivity, while also seeking evidence of stability across contexts and times. Seventy‐two mothers and their 10‐month‐olds participated in a procedure that included two episodes of Floor Play and Reunions following maternal differential treatment. Mothers were scored on contingent responsivity and warmth. At 12 months, the dyads underwent the Strange Situation Procedure where sensitivity was assessed using a 72‐item version of the MBQS. The findings revealed the stability of maternal sensitivity across times, contexts, and measures. However, linkages applied only to 10‐month scores from reunion, not play, episodes, supporting Pederson and Moran's (1995) assertion that high‐demand circumstances reveal more meaningful differences in maternal sensitivity. Copyright © 2012 John Wiley & Sons, Ltd.     

Using the Actor-Partner Interdependence Model to assess maternal and infant contributions to mother-infant affective exchanges during the Still-Face Paradigm

This study describes maternal and infant contributions to dyadic affective exchanges during the Still-Face Paradigm (SFP) in an understudied mostly low-income sample. One hundred eleven mothers and their 7-month-old infants were videotaped during the SFP to analyze how a social stressor affects mother-infant positive and negative affective exchanges during interaction. The SFP includes 3 episodes: baseline, maternal still-face, and reunion. Maternal and infant positive and negative affect were scored by masked reliable coders. Data were analyzed using the Actor-Partner Interdependence Model to test the hypotheses that each partner’s affectivity during the baseline episode would predict their own affectivity during the reunion episode (actor effects). We also expected that each partner’s affectivity during the baseline episode would influence the other partner’s affectivity during the reunion episodes (partner effects). After controlling for infant sex and maternal education, results provided evidence for actor effects for maternal and infant positive affect, and for partner effects for maternal baseline positive affect to infant positive affect during the reunion. One significant partner effect was observed for negative affect: Infant negativity during baseline predicted greater maternal negativity during reunion. Findings confirm that both mothers and infants contribute to dyadic affective processes during the SFP but specific findings vary depending on the affective valence in question. Clinical implications and future research are discussed.     

Positive affect moderates inhibitory control and positive affect following a single bout of self-select aerobic exercise

PurposeResearch suggests that individual differences in baseline cognitive performance moderates subsequent cognitive benefits following a single bout of exercise. The present study seeks to evaluate additional moderating mental states – specifically positive affect – on inhibitory control and affect following exercise.MethodsUsing a within- and between-participants pre-post cross-over design, eighty university students (54 females; 21.7 ± 2.7 years old) completed a flanker task and affect measures before and after a single bout of aerobic exercise at a self-selected intensity or studying for class (15-min) on separate days. Groups of high-positive affect (HPA; n = 41) and low-positive affect (LPA; n = 39) were determined based on a median split of positive affect measures prior to the exercise bout.ResultsThe HPA group revealed shorter reaction time (RT) from before to after exercise and rest with no difference observed between exercise and rest. The LPA group revealed shorter RT after exercise compared to before exercise and after rest. For accuracy, the LPA group improved performance during the exercise session compared to the rest session to a level comparable to the HPA group. Lastly, positive affect decreased in the LPA and HPA groups from before to after rest; however, only the LPA group’s positive affect increased from before to after exercise.ConclusionIndividuals with low positive affect experience greater cognitive and positive affect improvements following acute aerobic exercise at a self-select intensity, further supporting intraindividual differences in mental states as a mechanism for subsequent cognitive and affective benefits encompassing healthy behaviors of exercise.     

Emergency Training with Mothers Who Are Mentally Retarded

The purpose of the present article was to develop and validate a tool to assess knowledge of how to respond to common home emergencies and to validate a training program for mothers with mental retardation on how to respond to emergencies. Four mildly mentally retarded mothers were trained following a multiple baseline procedure in which one emergency at a time was introduced. Two of the mothers acquired most of the information for all of the emergencies and were able to apply the skills in a role playing situation. One mother dropped out before followup and the other mother had difficulty in acquisition, losing most of the gains after followup. While these results are encouraging, further work is needed with larger samples. Other research also should examine the relationship between maternal characteristics and acquisition of both knowledge and skill.     

PARENT EDUCATION PROJECT III: INCREASING AFFECTION AND RESPONSIVITY IN DEVELOPMENTALLY HANDICAPPED MOTHERS: COMPONENT ANALYSIS,GENERALIZATION, AND EFFECTS ON CHILD LANGUAGE

We evaluated the effects of a parent training program consisting of verbal instruction, modeling, and feedback on the affection and responsivity of 3 developmentally handicapped mothers towards their children. The results indicated the following: First, the training package increased maternal physical affection, praise, and imitation of child vocalizations. These parenting skills increased to levels found in comparison groups of nonhandicapped mothers. Second, the training package was more effective than verbal instruction alone, the latter being the predominant method presently used by social service workers. Third, most maternal gains were maintained over a 3- to 18-month follow-up period, although one mother required a reinforced maintenance procedure. Fourth, instructing mothers to generalize served to increase the generalization of newly acquired skills from play times (the training context) to child-care tasks (e.g., diapering, feeding). Fifth, teaching the parents to imitate child vocalizations was related to gains in both the frequency and quality of verbal behavior of the two language delayed children as measured by standardized developmental tests and in vivo comparisons with age-matched children (who had nonhandicapped parents). These results show that behavioral instruction can improve important child-rearing skills of developmentally handicapped mothers, with corresponding benefits to their children.     

Father,Mother, Brother,Sister: Primacy and Familial Language

From its inception Christianity has employed familial language to help believers frame their relationships, first to God, who was their common ‘Father’, and to one another. In the early church this was also true of bishops, and especially to the Patriarchs of Rome and Constantinople, where one is struck by the frequent use of fraternal language in order to establish their respective positions within the church. However, by the medieval period a shift took place whereby Rome began to reference itself not as the ‘brother’ or ‘sister’ of other churches but as ‘mother’ and ‘father’. Calls to reunion were thus increasingly framed in terms of filial obedience, with the return of the prodigal son becoming the West’s chief paradigm for understanding reunion. This continued for centuries, until the mid‐twentieth century, when Rome once again began to employ fraternal language in its dealings with the Orthodox.     

Parent-infant synchrony and the social-emotional development of triplets

To study the social-emotional development of triplets, 23 sets of triplets, 23 sets of twins, and 23 singleton infants (N=138) were followed from birth to 2 years. Maternal depression and social support were assessed in the postpartum period, mother-infant and father-infant interaction and the home environment were observed at 3 months, a separation-reunion episode and a maternal interview were conducted at 12 months, and infant behavior problems were evaluated at 24 months. Lower parent-infant synchrony was observed for triplets. Triplets showed less distress during maternal separation and less approach at reunion. Mothers reported lower adjustment and differentiation among siblings for triplets than for twins. Higher internalizing problems were reported for triplets, and the triplet with intrauterine growth retardation showed the poorest outcomes. Behavior problems were predicted by medical risk, maternal depression, parent-infant synchrony, infant approach, and mother adjustment. Discussion focuses on developmental risk when the exclusivity of the parent-infant relationship is compromised.     

Predicting maternal sensitivity: The roles of postnatal depressive symptoms and parasympathetic dysregulation

Previous research has established that maternal depression is a risk factor for a variety of negative developmental outcomes among infants and children. Although low levels of maternal sensitivity have been hypothesized to explain this risk, the biological mechanisms underlying the association between maternal depressive symptoms and low levels of maternal sensitivity have been largely underexplored. This study examined the roles of postnatal depressive symptoms and parasympathetic nervous system functioning as predictors of low levels of maternal sensitivity, during a stressful mother–infant interaction—the reunion phase of the Still‐Face Paradigm. Depressive symptoms and traitlike predispositions toward parasympathetic dysregulation, as indexed by low resting levels of respiratory sinus arrhythmia, were associated independently with less sensitive parenting. Discussion considers that during stressful mother–infant interactions, both mothers with depressive symptoms and mothers predisposed to parasympathetic dysregulation may have fewer emotional, physiological, and psychological resources with which to respond sensitively to their infants' cues.     

Family conflict is associated with longitudinal changes in insular‐striatal functional connectivity during adolescent risk taking under maternal influence

Maternal presence has marked effects on adolescent neurocognition during risk taking, influencing teenagers to make safer decisions. However, it is currently unknown whether maternal buffering changes over the course of adolescence itself, and whether its effects are robust to individual differences in family relationship quality. In the current longitudinal study, 23 adolescents completed a risk‐taking task under maternal presence during an fMRI scan before and after the transition to high school. Behavioral results reveal that adolescent risk taking increased under maternal presence across a one‐year period. At the neural level, we found that adolescents reporting higher family conflict showed longitudinal increases in functional coupling between the anterior insula (AI) and ventral striatum (VS) when making safe decisions in the presence of their mother, which was associated with increased real‐world risk taking. These findings show that individual differences in family relationship quality undermine effective development of AI‐VS connectivity resulting in increased risk taking.     

Stimulus control of maternal responsiveness to Norway rat (Rattus norvegicus) pup ultrasonic vocalizations

Mother rats (Rattus norvegicus; 6 to 8 days postpartum) approach and maintain proximal orientation to a pup that is emitting ultrasonic vocalizations (USVs) far more than do virgin females (W. J. Farrell & J. R. Alberts, 2002). We used a playback regimen to examine the roles of acoustic and nonacoustic cues in regulating maternal proximal orientation toward vocalizing pups. When presented with recorded USVs, mothers of 6- to 8-day-old pups and nulliparous virgin females exhibited equivalent levels of proximal orientation toward the playback speaker. Mothers did show enhanced proximal orientation toward recorded USVs, however, if a silent pup was positioned below the speaker. Pup odors appear to be crucial for the maternal response to vocalizing pups, as peripherally induced anosmia attenuated maternal proximal orientation toward a vocalizing pup. Furthermore, spatial contiguity between olfactory and auditory stimuli was required for a maximal maternal response.     

The role of the accessory and main olfactory systems in maternal behavior of the primiparous rat

The objective of this study was to analyze the respective roles of the main and accessory olfactory systems in the development of maternal behavior in the primiparous Wistar rat. Females underwent one of the following treatments: vomeronasal nerve section (VN), irrigation of nasal cavities with 5% ZnSO4 solution (ZN), surgical control, saline irrigation control, and normal control. Surgical or first irrigation were done before mating occurred. Irrigations were done every 7 days thereafter. The dams and their litters were observed from the day the litter was born (Day 1) through Day 16. Pup weights and temperatures were recorded daily. Home cages were checked daily for changes in nest location and number of times pups were found out of the nest. Retrieving tests were conducted on Days 4, 7, 10, and 13. The following behavioral items were observed: number of pup retrievals , number of times mother nosed or licked pups, percentage of litter returned to nest by end of test, dam self-grooming, dam climbing or rising, and dam digging or burrowing in shavings. The VN dams and their litters were not significantly different from the control dams and their litters on any of the measures taken. The ZN dams and their litters were not significantly different from their controls on all measures except for pup body temperature which was slightly lower from Day 13 through day 16 and pup body weight which was slightly lower from Day 12 through Day 16. Since these differences are very small, they do not seem to indicate a serious deficiency in maternal behavior. The results indicate that adequate maternal behavior develops with either of the two systems intact.     

Attachment in low‐SES rural Appalachian infants: Contextual,infant, and maternal interaction risk and protective factors

Attachment classifications were obtained for 95 low‐socioeconomic‐status (SES) rural Appalachian infants in the Strange Situation procedure at 15 months. The distribution of secure (B) and insecure (A, C, D) infants was similar to other low‐SES samples and significantly different from low‐risk samples. Levels of contextual and infant risk, together with maternal responsiveness to crying and pattern of sensitivity from 4 to 9 months, predicted attachment security. High social support, when examined as a protective factor, related to reduced contextual risk, but not to increased likelihood of security. Exploratory discriminant function analyses showed that infants in secure relationships differed in positive directions on contextual and maternal interactional factors. Insecure‐organized (A and C) infants experienced contextual and maternal interaction risks, while insecure‐disorganized (D) infants were best distinguished by infant characteristics, including greater likelihood of being male and low use of mother as a secure base at 9 months. ©2001 Michigan Association for Infant Mental Health.