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While most pup-naïve adult female mice can display, or be induced (by repeated exposure to pups) to display parental behavior rapidly, adult males are infanticidal or nonparental. The medial prefrontal cortex (mPFC) participates in attentional selection, decision-making, behavioral flexibility, and planning that may be critical in the rapid display of parental or infanticidal behavior. We investigated if NMDA-induced lesions in the mPFC (targeting prelimbic cortex) inhibited maternal or infanticidal behavior in pup-naïve adult female and male mice (C57BL/6), respectively. All Control females displayed full maternal behavior at the first encounter with pups. Lesioned female groups were partially maternal (50%) or nonmaternal (50%). Five repeated exposures of 60-min to pups were needed to induce full maternal behavior in female NMDA-lesioned groups. Control and lesioned males did not show significant differences. Control males displayed nonparental (17%) or infanticidal (83%) behavior, while all lesioned males were infanticidal. There was no difference in general locomotor and exploratory activity (i.e., peripheral crosses, rearings, immobility time) in female or male groups. Nevertheless, females and males of lesioned groups showed a reduction in the number of central crosses and time in the central area of an open field respectively, suggesting an increase in anxiety. Our results show that the mPFC is engaged in the rapid onset of maternal behavior in females, contributing with the motivation and planning of its rapid execution, or reducing the anxiety to the first encounter with pups. In contrast, infanticidal behavior, likely a more impulsive behavior, might require less planning from the mPFC. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Most species have predominant forms of social and reproductive behavior driven by many years of selection pressures and evolution. For example, rodent species can live in small or large groups, behave more tolerant or aggressively toward conspecifics (including newborns), and form or not bonds with other members of the group (including sexual partners). Any of those behavioral adaptations could result in good fitness for the species, but could also require compromises such as sharing resources, greater parental investment, increased risk of predation, etc. We propose that the oxytocin (OXT) system, among others neuroendocrine peptides, is at the basis of a neural mechanism that adapts and predisposes species to a particular social and reproductive form of living. In this review we will show evidence that the variability in the density of receptors for OXT (OXTR) in the nucleus accumbens (NAc) and the lateral septum (LS) predisposes species to adopt at least 4 different social and reproductive strategies in rodents. Large or medium size groups with lower conspecific spacing (preferred separation distance maintained by adult conspecifics), and high levels of promiscuity are characterized by low levels of OXTR in the NAc and LS (e.g. Ratus norvegicus, Ctenomys sociabilis, Scotinomys teguina, Cavia porcellus); small size groups with higher conspecific spacing and low levels of promiscuity are characterized by high OXTR in the NAc and the LS (e.g. Peromyscus californicus); large or medium groups with lower conspecific spacing and low levels of promiscuity characterized by high levels of OXTR in the NAc but low levels in the LS (e.g. Microtus ochrogaster, Heterocephalus glaber, Microtus kikuchii); and small or medium size groups with higher conspecific spacing and high levels of promiscuity characterized by low levels of OXTR in the NAc and high OXTR in the LS (e.g. Mus musculus, Ctenomys haigi, Peromyscus maniculatus, Microtus pennsylvanicus, Microtus montanus). Careful analysis of the distribution of OXTR, and other peptides receptors, in the brain can contribute to understand its function but also to predict reproductive and social strategies of species.

Naive female mice are usually described as spontaneously maternal. We investigated how many exposures to pups (15 min vs. 1 hr) were needed to induce full maternal behavior (FMB) in 20–22, 30–35, 60–65-days-old naive female mice (C57BL/6), and how cohabitation with the parturient mother and newborn siblings facilitated juvenile maternal behavior (MB). Only 20% of the adults displayed FMB immediately after the first exposure to pups. Incomplete MB was present in 11%, 20%, and 30% of juveniles, adolescents and adults, respectively. Three-sixty minute exposures to pups induced FMB in all adult subjects. All naive juveniles that were not exposed to their siblings and maternal fluids failed to show maternal behavior. In contrast, more than half of the juveniles present at their homecage during delivery of a second litter showed incomplete MB (34.5%) or FMB (21.5%) when tested individually housed in a novel cage. This study suggests that most adult female mice are not spontaneously maternal but gradually sensitized. Besides, naive juveniles could be inhibited or not motivated to show MB, but display adult-like behavior toward pups if previously exposed to newborn siblings and maternal fluids. © 2015 Wiley Periodicals, Inc. Dev Psychobiol 57: 189–200, 2015.

Maternal–infant interaction and behaviors are adapted to reduce the risk of predation and increase the probability of survival of the species. We determined how mother–young encounters and communication change by the development of the fawn (locomotion and feeding) throughout lactation in pampas deer (Ozotocerus bezoarticus). We registered the behavior of mother–fawn dyads for the first 60 postnatal days. Our results revealed three main developmental stages in the fawn, hiding (~0–19 days), active (~20–39 days), and adult-like (~40–60 days). In the hiding stage, the fawn stayed hidden, closer to the mother, and spent less time active, the mothers vocalized more often than the fawn, licked the fawns intensively while nursing, and were responsible for initiating nursing. In the active stage, licking behavior and vocalizations of the mother decreased while the fawns ate solid food, initiated nursing bouts, and displayed bursts of running activity. Finally, in the adult-like stage, the fawn showed many signs of nutritional weaning, and similar patterns of activity to their mothers. However, the duration and frequency of nursing bouts were unchanged during the study. We described mother–fawn interaction in pampas deer for the first time, and found that increased running activity in fawns anticipates nutritional weaning. Our results also suggest that to adapt to the development of the fawn, mothers only modify the dynamics of interaction and encounters rather than the time invested in nursing, an activity that also plays a role in maintaining mother–young affiliation.

Both animal and human studies have provided conclusive evidence that oxytocin (OXT) acts in the brain (eg, medial preoptic area, ventral tegmental area, nucleus accumbens) to promote parental behaviour under different reproductive and physiological conditions. OXT appears to accelerate and strengthen the neural process that makes newborns attractive or rewarding. Furthermore, OXT reduces stress/anxiety and might improve mood and well being, resulting in indirect benefits for parents. However, OXT also plays a role in the development of species reproductive and social strategies, making some species or individuals more prone to display caring activities in nonreproductive contexts. There are important differences in the development of the OXT system and its regulation by gonadal hormones that can make individuals or species very different. Those intra- and interspecific differences in the OXT system have been associated with differences in parental behaviour. For example, differences in OXT levels in body fluids and genetic variants for the OXT and OXT receptor genes have been associated with variability in parental mood and behaviour in humans. Thus, OXT has received much attention as a potential therapeutic agent for affective, emotional and behavioural problems. Despite many preliminary studies indicating promising findings, several unknown aspects of the OXT system remain to be addressed before we can achieve a complete understanding of its function in the brain. The enormous interest that this area of study has attracted in the last decade will likely continually contribute to advancing our understanding of the role of OXT in parental behaviour and other behavioural and physiological functions.

This article is part of a Special Issue "Parental Care". There is significant variability in the behavioral responses displayed by naive young and adult mice when first exposed to pups. This variability has been associated with differences in the expression of oxytocin receptors (OXTRs) in the brain in several species. Experiment I investigated the behavioral responses of juvenile, adolescent, and adult CB57BL/6 males and females when first exposed to pups. We found an age increase in maternal females (11% of juveniles, 20% of adolescents, and 50% of young adults), and infanticidal males (0% of juveniles, 30% of adolescents, 44.5% of young adults, and 100% of older adults). Experiment II investigated OXTR density in the brain of juvenile and adult mice. Our results revealed an age decline in the density of OXTR in several brain regions, including the lateral septum, cingulated and posterior paraventricular thalamic nucleus in both males and females. Adult females had higher OXTR density in the ventromedial nucleus/postero-ventral hypothalamus (VMH) and the accessory olfactory bulb (AOB), but lower density in the ventral region of the lateral septum (LSv) than juveniles. Males had lower OXTR density in the anterior olfactory area (AOA) compared to juveniles. No age or sex differences were found in the medial preoptic area, and amygdaloid nuclei, among other brain regions. This study suggests that 1) maturation of parental and infanticidal behavioral responses is not reached until adulthood; 2) the pattern of development of OXTR in the mouse brain is unique, region specific, and differs from that observed in other rodents; 3) either up or down regulation of OXTR in a few brain regions (VMH/AOB/LSv/AOA) might contribute to age or sex differences in parental or infanticidal behavior.

The neuropeptide oxytocin has been implicated in the regulation of affiliative behavior and maternal responsiveness in several mammalian species. Rodent species vary considerably in the expression of juvenile alloparental behavior. For example, alloparental behavior is spontaneous in juvenile female prairie voles (approximately 20 days of age), takes 1-3 days of pup exposure to develop in juvenile rats, and is nearly absent in juvenile mice and meadow voles. Here, we tested the hypothesis that species differences in pup responsiveness in juvenile rodents are associated with oxytocin receptor (OTR) density in specific brain regions. We found that OTR density in the nucleus accumbens (NA) is highest in juvenile prairie voles, intermediate in juvenile rats, and lowest in juvenile mice and meadow voles. In the caudate putamen (CP), OTR binding was highest in prairie voles, intermediate in rats and meadow voles, and lowest in mice. In contrast, the lateral septum (LS) shows an opposite pattern, with OTR binding being high in mice and meadow voles and low in prairie voles and rats. Thus, alloparental responsiveness in juvenile rodents is positively correlated with OTR density in the NA and CP and negatively correlated with OTR density in the LS. We then investigated whether a similar receptor-behavior relationship exists among juvenile female prairie voles by correlating individual variation in alloparental behavior with variation in OTR density. The time spent adopting crouching postures, the most distinctive component of alloparental behavior in juveniles, was positively correlated with OTR density in the NA (r = 0.47) and CP (r = 0.45) and negatively correlated with OTR density in the lateral septum (r = -0.53). Thus, variation in OTR density in the NA, CP, and LS may underlie both species and individual differences in alloparental care in rodents.

Oxytocin and the nucleus accumbens have been extensively implicated in the regulation of maternal behavior, and the processing of pup-related stimuli relevant for this behavior. Oxytocin receptor density in the nucleus accumbens is highly variable in virgin female prairie voles, as is their behavioral response to pups, ranging from neglecting and infanticidal to full maternal behavior. We hypothesized that oxytocin receptor in the nucleus accumbens facilitates the expression of "spontaneous" maternal behavior in prairie voles. Forty sexually-naive adult females were exposed to pups for the first time and tested for maternal behavior. Oxytocin receptor binding in the nucleus accumbens and other brain regions was later determined using autoradiography. Females that showed maternal behavior (lick and groom the pups and hover over them for at least 30 s, n=24) had higher oxytocin receptor density in the nucleus accumbens (shell subregion) (P

Juvenile female prairie voles (Microtus ochrogaster) are spontaneously maternal, while virgin adult females show significant variability in their response to first pup exposure, ranging from infanticidal to full maternal behavior. In the present study, we investigated whether differences in anxiety-like behavior and affiliation are associated with juvenile-adult and adult individual differences in the response to pups. Forty juvenile (19-20 days) and 42 adult (60-90 days) female prairie voles were exposed to pups for the first time and tested for maternal behavior, anxiety-like behavior (elevated plus maze, open field), and affiliation toward age-matched, same sex conspecifics. Juveniles displayed less anxiety-like behavior, were more affiliative to unfamiliar conspecifics, and interacted with pups more positively than adults. Adults that displayed maternal behavior spent less time immobile, made more crosses through the center of the open field arena, and were more affiliative than adults that attacked the pups. This suggests that lower locomotion or exploration in a novel environment and poor affiliative behavior are negatively associated with maternal responsiveness in female prairie voles.

Juvenile rats (18-23 days old) interact avidly with pups as novel stimuli and show maternal behavior after only 1-3 days of pup exposure; adults initially avoid pups and require 3-9 days of pup exposure. Upon exposure to pups as novel stimuli, adults had more c-Fos-immunoreactive neurons in the hypothalamus and amygdala--regions associated with aversion to pups--than adults exposed to familiar pup stimuli (maternal) or not exposed to pups (p < .05). In juvenile rats exposed to pups as novel stimuli, only the medial amygdala had a small significant increase of c-Fos neurons. In juveniles, this blunted engagement of c-Fos neurons may reflect the diminished activation of inhibitory neurons, facilitating the interaction of juveniles with pups as novel stimuli and onset of maternal behavior.

The molecular mechanisms underlying the evolution of complex behaviour are poorly understood. The mammalian genus Microtus provides an excellent model for investigating the evolution of social behaviour. Prairie voles (Microtus ochrogaster) exhibit a monogamous social structure in nature, whereas closely related meadow voles (Microtus pennsylvanicus) are solitary and polygamous. In male prairie voles, both vasopressin and dopamine act in the ventral forebrain to regulate selective affiliation between adult mates, known as pair bond formation, as assessed by partner preference in the laboratory. The vasopressin V1a receptor (V1aR) is expressed at higher levels in the ventral forebrain of monogamous than in promiscuous vole species, whereas dopamine receptor distribution is relatively conserved between species. Here we substantially increase partner preference formation in the socially promiscuous meadow vole by using viral vector V1aR gene transfer into the ventral forebrain. We show that a change in the expression of a single gene in the larger context of pre-existing genetic and neural circuits can profoundly alter social behaviour, providing a potential molecular mechanism for the rapid evolution of complex social behaviour.

Naïve female mice are usually described as spontaneously maternal. We investigated how many exposures to pups (15 min vs. 1 hr) were needed to induce full maternal behavior (FMB) in 20-22, 30-35, 60-65-days-old naïve female mice (C57BL/6), and how cohabitation with the parturient mother and newborn siblings facilitated juvenile maternal behavior (MB). Only 20% of the adults displayed FMB immediately after the first exposure to pups. Incomplete MB was present in 11%, 20%, and 30% of juveniles, adolescents and adults, respectively. Three-sixty minute exposures to pups induced FMB in all adult subjects. All naïve juveniles that were not exposed to their siblings and maternal fluids failed to show maternal behavior. In contrast, more than half of the juveniles present at their homecage during delivery of a second litter showed incomplete MB (34.5%) or FMB (21.5%) when tested individually housed in a novel cage. This study suggests that most adult female mice are not spontaneously maternal but gradually sensitized. Besides, naïve juveniles could be inhibited or not motivated to show MB, but display adult-like behavior toward pups if previously exposed to newborn siblings and maternal fluids.

Parental behavior is commonly displayed by progenitors. However, other individuals, genetically related (e.g. siblings, aunts, uncles) or not with the newborns, also display parental behavior (commonly called alloparental, or adoptive behavior). I hypothesize that species that live in family or social groups where other non-reproductive members (males and females) take care of infants, have brain adaptations to promote or facilitate that behavioral response. The present work revises the evidence supporting the hypothesis that high density of oxytocin receptors (OXTR) in the nucleus accumbens (NA) is one of those adaptations. All species known to have high NA OXTR show not only female, but also male alloparental care. Therefore, I predict that high NA OXTR could be present in all species in which juvenile and adult male alloparental behavior have been observed. Strategies to test this and other alternative working hypothesis and its predictions are presented.

Maternal behavior is expressed in different modalities, physiological conditions, and contexts. It is the result of a highly motivated brain, that allows the female to flexibily adapt her caring activities to different situations and social demands. To understand how mothers coordinate maternal and other motivated behaviors we discuss the limitations of current theoretical approaches to study maternal motivation (e.g. distinction between appetitive and consummatory behaviors), and propose a different approach (i.e. motorically active vs. passive motivations) and a distinction between maternal motivated state and maternal motivated behaviors. We review the evidence supporting dopamine mediation of maternal motivation and describe how different phases of the dopaminergic response - basal, tonic, and phasic release in the nucleus accumbens - relate to increased salience, invigorating behavior, and behavioral switching. The existing and new experimental paradigms to investigate maternal motivation, and its coexpression and coordination with other social or non-social motivations are also analyzed. An example of how specificity of motivational systems (e.g. maternal and sexual behavior at postpartum estrus) could be processed at the neural level is also provided. This revision offers new theoretical and experimental approaches to address the fundamental question of how mothers flexibly adapt and coordinate the different components of maternal behavior with other motivated behaviors, also critical for the survival of the species.

Maternal behavior is species-specific and expressed under different physiological conditions, and contexts. It is the result of neural processes that support different forms (e.g. postpartum, cycling sensitized and spontaneous maternal behavior) and modalities of mother-offspring interaction (e.g. maternal interaction with altricial/precocious young; selective/non-selective bond). To understand how the brain adapts to and regulates maternal behavior in different species, and physiological and social conditions we propose new neural models to explain different forms of maternal expression (e.g. sensitized and spontaneous maternal behavior) and the behavioral changes that occur across the postpartum period. We emphasize the changing role of the medial preoptic area in the neural circuitry that supports maternal behavior and the cortical regulation and adjustment of ongoing behavioral performance. Finally, we discuss how our accumulated knowledge about the psychobiology of mothering in animal models supports the validity of animal studies to guide our understanding of human mothering and to improve human welfare and health.

Naive female prairie voles show significant variability in their behavioral response to newborns. We investigated whether that behavioral response (a) was related to the quality of postpartum maternal behavior; (b) was affected by postpartum maternal experience; and (c) could be selectively bred. The behavior of females was recorded in three conditions: as naive in a nonreproductive context, as single lactating (no male present), and as experienced mother in a nonreproductive context. Finally, females and males with similar behavioral response to newborns were selectively bred for three generation. Males were removed before the offspring was born. Our results revealed that (a) naive females that attacked pups, spent more time distant from them after parturition than those that were maternal or ignored the pups (p

Social interactions among conspecifics are a fundamental and adaptively significant component of the biology of numerous species. Such interactions give rise to group living as well as many of the complex forms of cooperation and conflict that occur within animal groups. Although previous conceptual models have focused on the ecological causes and fitness consequences of variation in social interactions, recent developments in endocrinology, neuroscience, and molecular genetics offer exciting opportunities to develop more integrated research programs that will facilitate new insights into the physiological causes and consequences of social variation. Here, we propose an integrative framework of social behavior that emphasizes relationships between ultimate-level function and proximate-level mechanism, thereby providing a foundation for exploring the full diversity of factors that underlie variation in social interactions, and ultimately sociality. In addition to identifying new model systems for the study of human psychopathologies, this framework provides a mechanistic basis for predicting how social behavior will change in response to environmental variation. We argue that the study of non-model organisms is essential for implementing this integrative model of social behavior because such species can be studied simultaneously in the lab and field, thereby allowing integration of rigorously controlled experimental manipulations with detailed observations of the ecological contexts in which interactions among conspecifics occur.

Prairie voles ( Microtus ochrogaster ) are socially monogamous rodents that display high levels of affiliative behavior and biparental care. Both males and females contribute to the rearing of their offspring with minimal or no difference in their response to pups. Sexually naive prairie voles of both sexes also display spontaneous parental responses when exposed to pups in nonreproductive contexts. This spontaneous parental response includes licking, grooming, and hovering over the pups immediately after the first exposure, as well as subsequent nest building, and retrieval. However, there is significant variability in parental responsiveness both within and across populations. According to studies and others using different populations of prairie voles, most males (70–80%) display spontaneous parental care, and a small percentage (10–20%) generally ignore or neglect the pups. Infanticidal responses in males are not uncommon but occur in only 10% of the cases. Sexually naive female prairie voles, by contrast, are much more variable in their response to pups than males. About 50–60% of female prairie voles show spontaneous maternal responses when first exposed to pups, while about 40–50% either ignore/neglect the pups or display infanticidal behavior when exposed to them. It is found that variation in the response to pups in naive females is associated with variation in measures of emotionality and nonmaternal affiliative behavior. Adult females that display maternal behavior spend less time immobile, and make more crosses through the center of an open field arena than females that attack pups. This observation suggests that females that display less anxiety-like behavior and/or increased exploratory behavior are more likely to interact positively with novel pups.

Continuous exposure of non-parturient rats to pups can induce maternal behavior similar in most aspects to that found in the postpartum rat. Surprisingly, young juvenile rats (20-24 days of age) only require 1-3 days of exposure to pups, while adults require 4-8 days before maternal behavior emerges. Dopamine (DA) and possibly serotonin (5-HT) may mediate the expression of adult maternal behavior. We hypothesize that postnatal changes in DA and 5-HT within the neural circuit that supports maternal behavior including the medial preoptic area (MPOA), medial and cortical amygdala (MCA), and nucleus accumbens (NAC), may underlie these differences in responsiveness across juveniles and adults. We measured DA, 5-HT, and their metabolites in postmortem samples of these regions in maternal and non-maternal juvenile and adult females. The only difference found across behavioral groups was that the MPOA of adults induced into maternal behavior by pup exposure had more DA than did that of isolated adult females or maternal juveniles. However, when adults versus juveniles were compared, the content of DA and 3,4-dihydroxyphenylacetic (DOPAC) was higher in the adult than in the juvenile NAC and MCA; the content of 5-HT and 5-hydroxyindoleacetic acid (5-HIAA) in these structures did not vary across the age groups. In contrast, higher levels of 5-HT and 5-HIAA were found in the MPOA in juveniles compared to adults. We propose that these region-specific age differences in DA and 5HT may underlie differences in juvenile-adult responses to pups.

Small neurotoxin lesions in the medial preoptic area (MPOA) block maternal behavior (MB) in adults but large lesions are required to produce the same effect in juvenile rats (23-27 days of age). To study the maturation of MPOA control of MB, in Experiment I, we compared the effects of small versus large neurotoxin MPOA lesions at midpuberty (38 days of age) on MB. Midpubertal females with large MPOA lesions showed severe impairment in MB affecting retrieving, crouching, and nest building, but 85% of females with small MPOA lesions exhibited all components of MB and performed like control females without MPOA lesions. To study the role of ovarian hormones during puberty on the maturation of MPOA mediation of MB (Experiment IIA), females were ovariectomized either before or after puberty and small MPOA cytotoxic lesions were made at 53 days of age. At 60 days of age both groups showed similar deficits in MB which indicated that the maturation of the MPOA mediation of MB is not dependent on pubertal ovarian hormones. In Experiment IIB, we administered estradiol benzoate (sc) and this overcame the deficit in MB after small MPOA lesions in females that had been deprived of estrogen for shorter periods (30 days) but had not been deprived for longer periods (60 days). In addition, ovary-intact females with circulating estrogen and small lesions in the MPOA at 53 days of age did not show deficits in MB.

OLAZABAL, D. E. AND A. FERREIRA. Maternal behavior in rats with kainic acid-induced lesions of the hypothalamic paraventricular nucleus. PHYSIOL BEHAV 61 (5) 779–784, 1997.—The rat maternal behavior consists of different pup-caring activities, such as retrieving, licking, and crouching. Mothers also build a nest, consume more food, are more aggressive, and show less fear behavior than in other stages of the reproductive cycle. It has been reported that oxytocin (OT) and the milk-ejection pathway could be involved in modulating maternal behavior. The paraventricular nucleus (PVN) of the hypothalamus forms part of the milk-ejection pathway and is also the major source of OT release in the brain. Kainic acid (KA) lesions (0.5 μ g/0.5 μ l) in the PVN performed on day 2 after parturition, affected retrieving behavior in the mother rat and produced a decrease in pups' weight gain. Because KA destroys only cell bodies, the changes that we observed could be due to the local destruction of neurons, rather than that of the fibers of passage. No alteration was observed in other components of the pup-caring activities, food intake, aggressive behavior, and fear in the lesioned mothers.

The pampas deer (Ozotoceros bezoarticus) is a South American grazing deer which is in extreme danger of extinction. Very little is known about the biology of the pampas deer. Moreover, most information has not been published in peer-reviewed scientific journals, and is only available in local publications, theses, etc. Therefore, our aim was to update and summarize the available information regarding the reproductive biology of the pampas deer. Moreover, in most sections, we have also included new, unpublished information. Detailed descriptions are provided of the anatomy of both the female and the male reproductive tract, puberty onset, the oestrous cycle and gestational length. Birthing and the early postpartum period are described, as are maternal behaviour and early fawn development, seasonal distribution of births, seasonal changes in male reproduction and antler cycle, reproductive behaviour, semen collection, and cryopreservation. Finally, an overview is given and future directions of research are proposed.