Anxious about rejection, avoidant of neglect: Infant marmosets tune their attachment based on individual caregiver's parenting style.

Children's secure attachment with their primary caregivers is crucial for physical, cognitive, and emotional maturation. Yet, the causal links between specific parenting behaviors and infant attachment patterns are not fully understood. Here we report infant attachment in New World monkeys common marmosets, characterized by shared infant care among parents and older siblings and complex vocal communications. By integrating natural variations in parenting styles and subsecond-scale microanalyses of dyadic vocal and physical interactions, we demonstrate that marmoset infants signal their needs through context-dependent call use and selective approaches toward familiar caregivers. The infant attachment behaviors are tuned to each caregiver's parenting style; infants use negative calls when carried by rejecting caregivers and selectively avoid neglectful and rejecting caregivers. Family-deprived infants fail to develop such adaptive uses of attachment behaviors. With these similarities with humans, marmosets offer a promising model for investigating the biological mechanisms of attachment security.

Effects of oxytocin ablation on pup rescue, nursing behaviors and response to pup separation in early-to-mid postpartum mice.

Oxytocin, a neuropeptide hormone, is indispensable for milk ejection during nursing and is important for uterine contractions during parturition. The exact functions of oxytocin in postpartum maternal behaviors and motivations require further investigation. To this end, we characterized the role of oxytocin in components of maternal motivations during the mid-postpartum period, which has not been previously studied. To maintain suckling stimuli, postpartum oxytocin knockout (Oxt-/- ) and heterozygous (Oxt+/- ) littermates were co-housed with a wild-type lactating mother and its litter, and were examined for their ability to retrieve pups under standard or high-risk conditions, nursing behavior, maternal aggression towards an unfamiliar intruder, and motivation to regain contact with separated pups. One-third of Oxt-/- mothers exhibited prolonged parturition but were otherwise grossly healthy. Despite their inability to eject milk, Oxt-/- mothers displayed nursing behaviors for similar durations to Oxt+/- mothers during the second postpartum week. In addition, Oxt-/- mothers were essentially intact for pup retrieval under standard conditions and were motivated to stay close to pups, although they showed a mild decrease in maternal care under high-risk conditions and increased anxiety-like behaviors in pup-related contexts. The present findings indicate that oxytocin is dispensable for nursing behavior and maternal motivations, yet suggest that oxytocin may be relevant for stress resilience in the postpartum period.

A method to soothe and promote sleep in crying infants utilizing the transport response.

Approximately 20%-30% of infants cry excessively and exhibit sleep difficulties for no apparent reason, causing parental stress and even triggering impulsive child maltreatment in a small number of cases.1-8 While several sleep training methods or parental education programs may provide long-term improvement of infant cry and sleep problems, there is yet to be a conclusive recommendation for on-site behavioral interventions.9-13 Previously we have reported that brief carrying of infants transiently reduces infant cry via the transport response, a coordinated set of vagal activation and behavioral calming conserved in altricial mammals.14-18 In this study, we disentangled complex infant responses to maternal holding and transport by combining subsecond-scale, event-locked physiological analyses with dynamic mother-infant interactions. Infant cry was attenuated either by maternal carrying or by reciprocal motion provided by a moving cot, but not by maternal holding. Five-minute carrying promoted sleep for crying infants even in the daytime when these infants were usually awake, but not for non-crying infants. Maternal laydown of sleeping infants into a cot exerted bimodal effects, either interrupting or deepening the infants' sleep. During laydown, sleeping infants were alerted most consistently by the initiation of maternal detachment, then calmed after the completion of maternal detachment in a successful laydown. Finally, the sleep outcome after laydown was associated with the sleep duration before the laydown onset. These data propose a "5-min carrying, 5- to 8- min sitting" scheme for attending to infant cry and sleep difficulties, which should be further substantiated in future studies. VIDEO ABSTRACT.

Oxytocin Facilitates Allomaternal Behavior under Stress in Laboratory Mice.

Oxytocin (Oxt) controls reproductive physiology and various kinds of social behaviors, but the exact contribution of Oxt to different components of parental care still needs to be determined. Here, we illustrate the neuroanatomical relations of the parental nurturing-induced neuronal activation with magnocellular Oxt neurons and fibers in the medial preoptic area (MPOA), the brain region critical for parental and alloparental behaviors. We used genetically-targeted mouse lines for Oxt, Oxt receptor (Oxtr), vasopressin receptor 1a (Avpr1a), vasopressin receptor 1b (Avpr1b), and thyrotropin-releasing hormone (Trh) to systematically examine the role of Oxt-related signaling in pup-directed behaviors. The Oxtr-Avpr1a-Avpr1b triple knock-out (TKO), and Oxt-Trh-Avpr1a-Avpr1b quadruple KO (QKO) mice were grossly healthy and fertile, except for their complete deficiency in milk ejection and modest deficiency in parturition secondary to maternal loss of the Oxt or Oxtr gene. In our minimal stress conditions, pup-directed behaviors in TKO and QKO mothers and fathers, virgin females and males were essentially indistinguishable from those of their littermates with other genotypes. However, Oxtr KO virgin females did show decreased pup retrieval in the pup-exposure assay performed right after restraint stress. This stress vulnerability in the Oxtr KO was abolished by the additional Avpr1b KO. The general stress sensitivity, as measured by plasma cortisol elevation after restraint stress or by the behavioral performance in the open field (OF) and elevated plus maze (EPM), were not altered in the Oxtr KO but were reduced in the Avpr1b KO females, indicating that the balance of neurohypophysial hormones affects the outcome of pup-directed behaviors.

Calcitonin receptor signaling in the medial preoptic area enables risk-taking maternal care.

Maternal mammals exhibit heightened motivation to care for offspring, but the underlying neuromolecular mechanisms have yet to be clarified. Here, we report that the calcitonin receptor (Calcr) and its ligand amylin are expressed in distinct neuronal populations in the medial preoptic area (MPOA) and are upregulated in mothers. Calcr+ MPOA neurons activated by parental care project to somatomotor and monoaminergic brainstem nuclei. Retrograde monosynaptic tracing reveals that significant modification of afferents to Calcr+ neurons occurs in mothers. Knockdown of either Calcr or amylin gene expression hampers risk-taking maternal care, and specific silencing of Calcr+ MPOA neurons inhibits nurturing behaviors, while pharmacogenetic activation prevents infanticide in virgin males. These data indicate that Calcr+ MPOA neurons are required for both maternal and allomaternal nurturing behaviors and that upregulation of amylin-Calcr signaling in the MPOA at least partially mediates risk-taking maternal care, possibly via modified connectomics of Calcr+ neurons postpartum.

Using maternal rescue of pups in a cup to investigate mother-infant interactions in mice/rodents.

Efficient parental care is indispensable for survival of the mammalian offspring, and therefore both parents and offspring cooperate to achieve the best performance. For example, when parents transport altricial offspring, the offspring immediately respond by reducing its cry and movement in both human infants and rodent pups. This coordinated set of central, motor and cardiac responses is designated as the Transport Response (TR) and is shown to facilitate maternal carrying in rodents. The present study aims to investigate the core behavioural characteristics of mother-infant interaction, and to investigate the mechanisms underlying the mother-pup cooperation using pharmacological and genetic manipulations (i.e. Oprm1-/). Along with the clear developmental changes of the pups' immobility and posture during maternal carrying as previously reported, there were also adaptations in maternal strategies, particularly in positioning of foothold and oral grasp over the pup's body, with the pups' age and pup's behaviour. Tree-based models elucidated that both of these maternal variables as well as percentage of pups' struggle predict the time required for pup retrieval from a cup. When the sensory-motor control in pups was disturbed by pharmacological or genetic manipulations, these core behaviours were inefficiently performed and impede maternal retrieval. Mother-infant mutual fit is a complex construct where several intermingled mechanisms are involved. Thus mothers and infants, when interacting, should be considered together as one whole system in which any change in one side or the other, affects the output of the whole dyad. The outcome of the interaction relays on a specific dynamic pattern of infant and maternal behaviours, which mutually change and adapt to fit each other's needs. Key features to reach a successful outcome of the interaction were the maternal retrieving strategy and infants' Transport Response behaviour.

Sex-reversed correlation between stress levels and dominance rank in a captive non-breeder flock of crows.

Group living has both benefits and costs to individuals; benefits include efficient acquisition of resources, and costs include stress from social conflicts among group members. Such social challenges result in hierarchical dominance ranking among group members as a solution to avoid escalating conflict that causes different levels of basal stress between individuals at different ranks. Stress-associated glucocorticoid (corticosterone in rodents and birds; CORT) levels are known to correlate with dominance rank in diverse taxa and to covary with various social factors, such as sex and dominance maintenance styles. Although there is much evidence for sex differences in the basal levels of CORT in various species, the correlation of sex differences in basal CORT with dominance rank is poorly understood. We investigated the correlation between CORT metabolites (CM) in the droppings and social factors, including rank and sex, in a captive non-breeder group of crows. In this group, all the single males dominated all the single females, and dominance ranks were stable among single males but relatively unstable among single females. CM levels and rank were significantly correlated in a sex-reversed fashion: males at higher rank (i.e., more dominant) had higher CM, whereas females at higher rank exhibited lower CM. This is the first evidence of sex-reversed patterns of CM-rank correlation in birds. The results suggest that different mechanisms of stress-dominance relationships operate on the sexes in non-breeder crow aggregations; in males, stress is associated with the cost of aggressive displays, whereas females experience subordination stress due to males' overt aggression.