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Fos expression in the medial preoptic area and nucleus accumbens of female Japanese quail (Coturnix japonica) after maternal induction and interaction with chicks
Abstract
The neural system underlying maternal caregiving has often been studied using laboratory rodents and a few other mammalian species. This research shows that the medial preoptic area (mPOA) integrates sensory cues from the young that, along with hormonal and other environmental signals, control maternal acceptance of neonates. The mPOA then activates the mesolimbic system that drives maternal motivation and caregiving activities. How components of this neural system respond to maternal experience and exposure to young in non-mammals has rarely been examined. To gain more insight into this question, virgin female Japanese quail (Coturnix japonica) were induced to be maternal through four days of continuous exposure to chicks (Maternal), or were not exposed to chicks (Non-Maternal). Chicks were removed overnight from the Maternal group and half the females from each group were then exposed to chicks for 90 minutes (Exposed), or not exposed to chicks (Non-Exposed), before euthanasia. The number of Fos-immunoreactive (Fos-ir) cells was examined as a marker of neuronal activation. As expected, repeated exposure to chicks induced caregiving behavior in the Maternal females, which persisted after the overnight separation, suggesting formation of a maternal memory. In contrast, Non-Maternal females were aggressive and rejected chicks when exposed to them. Exposed females, whether or not they were given prior experience with chicks (i.e., regardless if they accepted or rejected chicks during the exposure before euthanasia), had more Fos-ir cells in the mPOA compared to Non-Exposed females. In the nucleus accumbens (NAC), the number of Fos-ir cells was high in all Maternal females regardless of whether or not they were Exposed to chicks again before euthanasia. In the lateral bed nucleus of the stria terminalis, a site involved in general stress responding, groups did not differ in Fos-ir cells. These data indicate a conserved role for the mPOA and NAC in maternal caregiving across vertebrates, with the mPOA acutely responding to the salience rather than valence of offspring cues, and the NAC showing longer-term changes in activity after a positive maternal experience even without a recent exposure.
... The mPOA is a crucial brain region responsible for integrating sensory and environmental inputs to modify social motivation and reward seasonally. The mPOA plays a wellestablished role in sexually motivated and maternal behaviors across vertebrates (Balthazart and Ball, 2007;Dominguez and Hull, 2005;Lonstein et al., 2021;Numan and Woodside, 2010), so it was not surprising to find that this role extended to sexually motivated song, with lesions to mPOA abolishing song in this context in male starlings (Alger et al., 2016;Alger et al., 2009;Alger and Riters, 2006;Riters and Ball, 1999). However, it was not expected that the mPOA would be critical for affiliative, rewarding behaviors outside a reproductive context. ...
Social motivation and reward are dynamic and flexible, shifting adaptively across contexts to meet changing social demands. This is exceptionally apparent when seasonal contexts are considered in seasonally breeding songbirds as they cycle from periods of sexual motivation and reward during the breeding season to periods of extreme gregariousness outside the breeding season when non-sexual social interactions gain reward value, motivating birds to form flocks. Here we review evidence demonstrating a key integrative role for the medial preoptic area (mPOA) in the seasonally-appropriate adjustment of behaviors, with seasonal changes in dopamine activity in mPOA adjusting social motivation and changes in opioid activity modifying social reward. Experiments demonstrate that dramatic seasonal fluctuations in steroid hormone concentrations alter patterns of opioid- and dopamine-related protein and gene expression in mPOA to modify social motivation and reward to meet seasonal changes in social demands. These studies of birdsong and seasonality provide new insights into neural and endocrine mechanisms underlying adaptive changes in social motivation and reward and highlight an underappreciated, evolutionarily conserved role for the mPOA in important social behaviors in non-reproductive contexts.
Evidence indicates there is a neural system that inhibits maternal behavior in virgin rats. It has been suggested that pregnancy hormones promote the onset of maternal behavior by reducing the behavioral influence of this system. The authors used c-Fos immunocytochemistry to identify brain regions more activated by pup exposure in nonmaternal rats than in maternal rats. Previous experiments indicated that some of these regions, such as the posterodorsal medial amygdala and several medial hypothalamic sites, inhibit maternal behavior. For others, such as the ventral lateral septum, dorsal premammillary nucleus, and principal bed nucleus of the stria terminalis, this is the first indication that they could also inhibit maternal responding. These regions have previously been implicated in promoting defensive behaviors, consistent with the finding that nonmaternal rats actively avoid pups. These findings suggest the existence of a neural circuit through which pup exposure could promote defensive responses in virgin rats, and how pregnancy hormones could reduce such activity to stimulate maternal behavior.
Parental care has evolved repeatedly and independently across animals. While the ecological and evolutionary significance of parental behaviour is well recognized, underlying mechanisms remain poorly understood. We took advantage of behavioural diversity across closely related species of South American poison frogs (Family Dendrobatidae) to identify neural correlates of parental behaviour shared across sexes and species. We characterized differences in neural induction, gene expression in active neurons and activity of specific neuronal types in three species with distinct care patterns: male uniparental, female uniparental and biparental. We identified the medial pallium and preoptic area as core brain regions associated with parental care, independent of sex and species. The identification of neurons active during parental care confirms a role for neuropeptides associated with care in other vertebrates as well as identifying novel candidates. Our work is the first to explore neural and molecular mechanisms of parental care in amphibians and highlights the potential for mechanistic studies in closely related but behaviourally variable species to help build a more complete understanding of how shared principles and species-specific diversity govern parental care and other social behaviour.
A growing number of studies implicate the brain's reward circuitry in aggressive behavior. However, the cellular and molecular mechanisms within brain reward regions that modulate the intensity of aggression as well as motivation for it have been underexplored. Here, we investigate the cell-type-specific influence of ΔFosB, a transcription factor known to regulate a range of reward and motivated behaviors, acting in the nucleus accumbens (NAc)-a key reward region-in male aggression in mice. We show that ΔFosB is specifically increased in dopamine D1 receptor (Drd1) expressing medium spiny neurons (D1-MSNs) in NAc after repeated aggressive encounters. Viral-mediated induction of ΔFosB selectively in D1-MSNs of NAc intensifies aggressive behavior, without affecting the preference for the aggression-paired context in a conditioned place preference (CPP) assay. In contrast, ΔFosB induction selectively in D2-MSNs reduces the time spent exploring the aggression-paired context during CPP without affecting the intensity of aggression per se. These data strongly support a dissociable cell-type-specific role for ΔFosB in the NAc in modulating aggression and aggression reward.Significance Statement:Aggressive behavior is associated with several neuropsychiatric disorders and can be disruptive for the individuals as well as their victims. Studies have shown a positive reinforcement mechanism underlying aggressive behavior that shares many common features with drug addiction. Here, we explore the cell-type-specific role of the addiction-associated transcription factor ΔFosB in the nucleus accumbens (NAc) in aggression. We found that ΔFosB expression promotes aggressive behavior, effects that are dissociable from its effects on aggression reward. This finding is a significant first step in identifying therapeutic targets for the reduction of aggressive behavior across a range of neuropsychiatric illnesses.
Parenting is essential for the survival and wellbeing of mammalian offspring. However, we lack a circuit-level understanding of how distinct components of this behaviour are coordinated. Here we investigate how galanin-expressing neurons in the medial preoptic area (MPOAGal) of the hypothalamus coordinate motor, motivational, hormonal and social aspects of parenting in mice. These neurons integrate inputs from a large number of brain areas and the activation of these inputs depends on the animal’s sex and reproductive state. Subsets of MPOAGal neurons form discrete pools that are defined by their projection sites. While the MPOAGal population is active during all episodes of parental behaviour, individual pools are tuned to characteristic aspects of parenting. Optogenetic manipulation of MPOAGal projections mirrors this specificity, affecting discrete parenting components. This functional organization, reminiscent of the control of motor sequences by pools of spinal cord neurons, provides a new model for how discrete elements of a social behaviour are generated at the circuit level. Galanin-expressing neurons in the medial preoptic area coordinate different aspects of motor, motivational, hormonal and social behaviour associated with parenting by projecting to different brain regions depending on the type of behaviour and sex and reproductive state of mice.
The medial preoptic area (mPOA) differs between males and females in nearly all species examined to date, including humans. Here, using fiber photometry recordings of Ca 2+ tran-sients in freely behaving mice, we show ramping activities in the mPOA that precede and correlate with sexually dimorphic display of male-typical mounting and female-typical pup retrieval. Strikingly, optogenetic stimulation of the mPOA elicits similar display of mounting and pup retrieval in both males and females. Furthermore, by means of recording, ablation, optogenetic activation, and inhibition, we show mPOA neurons expressing estrogen receptor alpha (Esr1) are essential for the sexually biased display of these behaviors. Together, these results underscore the shared layout of the brain that can mediate sex-specific behaviors in both male and female mice and provide an important functional frame to decode neural mechanisms governing sexually dimorphic behaviors in the future.
Correlation is a statistical technique which shows whether and how strongly two continuous variables are related. In this article, which is the eighth part in a series on ′Common pitfalls in Statistical Analysis′, we look at the interpretation of the correlation coefficient and examine various situations in which the use of technique of correlation may be inappropriate.
Unlabelled:
Brain-derived neurotrophic factor (BDNF), a member of the neurotrophin family, regulates both survival and differentiation of several neuronal populations in the nervous system during development, as well as synaptic plasticity in the adult brain. BDNF exerts its biological functions through its receptor TrkB. Although the regulation of BDNF transcription by neuronal activity has been widely studied, little is known about TrkB signaling-dependent expression of BDNF. Using rat primary cortical neuron cultures, we show that the BDNF gene is a subject to an extensive autoregulatory loop, where TrkB signaling upregulates the expression of all major BDNF transcripts, mainly through activating MAPK pathways. Investigating the mechanisms behind this autoregulation, we found that AP-1 transcription factors, comprising Jun and Fos family members, participate in the induction of BDNF exon I, III, and VI transcripts. AP-1 transcription factors directly upregulate the expression of exon I transcripts by binding two novel AP-1 cis-elements in promoter I. Moreover, our results show that the effect of AP-1 proteins on the activity of rat BDNF promoters III and VI is indirect, because AP-1 proteins were not detected to bind the respective promoter regions by chromatin immunoprecipitation (ChIP). Collectively, we describe an extensive positive feedback system in BDNF regulation, adding a new layer to the elaborate control of BDNF gene expression.
Significance statement:
Here, we show for the first time that in rat primary cortical neurons the expression of all major BDNF transcripts (exon I, II, III, IV, VI, and IXa transcripts) is upregulated in response to TrkB signaling, and that AP-1 transcription factors participate in the induction of exon I, III, and VI transcripts. Moreover, we have described two novel functional AP-1 cis-elements in BDNF promoter I, responsible for the activation of the promoter in response to TrkB signaling. Our results indicate the existence of a positive feedback loop for obtaining sufficient BDNF levels necessary for various TrkB signaling-dependent physiological outcomes in neurons.
The reproductive experience of pregnancy, lactation and motherhood can significantly remodel the female's biological state, affecting endocrine, neuroendocrine, neural, and immunological processes. The brain, pituitary gland, liver, thymus, and mammary tissue are among the structures that are modified by reproductive experience. The present review that focuses on rodent research, but also includes pertinent studies in sheep and other species, identifies specific changes in these processes brought about by the biological states of pregnancy, parturition, and lactation and how the components of reproductive experience contribute to the remodeling of the maternal brain and organ systems. Findings indicate that prior parity alters key circulating hormone levels and neural receptor gene expression. Moreover, reproductive experience results in modifications in neural processes and glial support. The possible role of pregnancy-induced neurogenesis is considered in the context of neuroplasticity and behavior, and the effects of reproductive experience on maternal memory, i.e. the retention of maternal behavior, together with anxiety and learning are presented. Together, these sets of findings support the concept that the neural and biological state of the adult female is significantly and dramatically altered on a long-term basis by the experiences of parity and motherhood. Remodeling of the maternal brain and other biological systems is posited to help facilitate adaptations to environmental/ecological challenges as the female raises young and ages.
Many species, including humans, engage in a series of behaviors that are preparatory to the arrival of offspring. Such "nesting behaviors" are of obvious importance, but relevant neuroendocrine mechanisms remain little studied. We here focus on the potential roles of vasoactive intestinal polypeptide (VIP) in the performance of appetitive and consummatory nesting behaviors in male and female zebra finches (Taeniopygia guttata). Using combined immunocytochemistry for Fos and in situ hybridization for VIP, we now show that many VIP cell groups show increased transcriptional activity in response to nest building in male and female zebra finches. Particularly strong data come from the preoptic area (medial preoptic area and medial preoptic nucleus), where VIP-Fos co-expression correlates positively with three different measures of nesting behavior, as does the number of VIP-expressing cells. Remarkably, we find that VIP mRNA and/or VIP-Fos co-expression is correlated with nesting behavior in virtually every brain area that we examined, including the medial amygdala (anterior and posterior), medial bed nucleus of the stria terminalis, medial preoptic area, medial preoptic nucleus, anterior hypothalamus, ventromedial hypothalamus, periaqueductal gray complex (central gray and nucleus intercollicularis), and ventral tegmental area. Near-significant effects are also obtained in the tuberoinfundibular hypothalamus. Although most correlations are positive, negative correlations are observed for the VIP cell group of the anterior hypothalamus, a population that selectively promotes aggression, and also the periaqueductal gray complex. These data demonstrate a network-wide relationship between peptide production and social behavior that is, to our knowledge, unparalleled by other peptidergic modulators.
Our study investigated relationships between a precocial bird's fearfulness and maternal care, and the implication of maternal care as a vector for non-genomic transmission of fearfulness to chicks. We compared care given to chicks between two sets of female Japanese quail selected to present either high (LTI) or low fearfulness (STI). Chicks, from a broiler line, were adopted by these females following a sensitization procedure. Chicks' fearfulness after separation from their mother was assessed by well-established procedures. LTIs took longer to present maternal responses, pecked chicks more during the first days post-hatch, presented impaired maternal vocal behaviour and were globally less active than STI females. Chicks mothered by LTIs presented more fearful reactions than did chicks mothered by STIs, supporting the hypothesis of a non-genetic maternal transmission of fearfulness. We suggest that the longer latencies required by LTIs to become maternal are a consequence of their greater fear of chicks, and that their lower general and vocal activity could be components of a heightened antipredatory strategy. We discuss the transmission of maternal fearfulness to fostered chicks, taking into account the possible implication of several well-known mechanisms underlying maternal effects.
Used Fos immunocytochemistry to show that the medial preoptic area and ventral bed nucleus of the stria terminalis are activated in maternally behaving female rats. In Exp 1, virgin female rats that showed maternal behavior toward pups had more cells in these regions that expressed Fos-like immunoreactivity than did virgin females that were not maternally responsive. In Exp 2, postpartum rats that were exposed to pups and showed maternal behavior had more Fos-labeled cells in these regions than did postpartum rats exposed to candy. Evidence also indicated that functional modifications in the medial amygdala were related to the changes in Fos expression observed in the preoptic area and ventral bed nucleus of the stria terminalis. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
Nest building in birds involves a behavioral sequence (nest material collection and deposition in the nest) that offers a unique model for addressing how the brain sequences motor actions. In this study, we identified brain regions involved in nesting behavior in male and female zebra finches (Taeniopygia guttata). We used Fos immunohistochemistry to quantify production of the immediate early gene protein product Fos (a molecular indicator of neuronal activity) in the brain and correlated this expression with the variation in nesting behavior. Using this technique, we found that neural circuitry involved in motor sequencing, social behavior, reward and motivation were active during nesting. Within pairs of nesting birds, the number of times a male picked up or deposited nesting material and the amount of time a female spent in the nest explained the variation in Fos expression in the anterior motor pathway, social behavior network, and reward neural circuits. Identification of the brain regions that are involved in nesting enables us to begin studying the roles of motor sequencing, context, and reward in construction behavior at the neural level.
Quails issued of migranyt parents show a large variability of their reproductive phenotypes when exposed in captivity to a winter Sahelian photoperiod (16º lat. N.). Fifteen per cent of these females lay spontaneously in December and/or January; 75% before late April.
In order to evaluate the possibility of this sexual precocity in natural conditions, we have measured the gonadal development and other sexual characteristics: song, cloacal development, pair formation of the European quail (Coturnix c. coturnix) populations wintering in the aluvial plains in the Centre (39-40º lat. N.) of Portugal. TRhe study was based on samples of birds shot there during the hunting seasons (September to December) of 1991, 1992, 1993 and 1994 (n=149).
Results indicate that these wintering populations are starting their sexual development in late autumn. Importance and chronology of this sexual precocity seem to be related with sex: males were sexually more advanced than females. Distinct results were obtained in diferent years and stations according to weather conditions (temperature): in December 1992 (cold winter) only 38% of the birds analysed i the coastal stations showed a beginning of sexual development, in contrast with 88% observed in December 1994.
A large proportion (46% males, 51% females) of the birds shot on coastal stations (any frozen day) showed signs of sexual precocity (more than 100 mg of gonadal weight). Only a few birds were concerned the same year in colder interior stations of Centre Portugal as Guadiana basin (0% males and 18% females).
Care provided by females of many mammal species varies naturally between individuals; these differences in turn influence the phenotypic development of their offspring. When individual maternal behavioural traits are consistent over a number of breeding periods, maternal styles can be defined. These styles have been studied in a large range of mammalian species. Nevertheless, mammals rarely offer the possibility to dissociate mothers' behavioural influence from their genetic influence or their physiological influence via lactation. Here, we provide, for the first time, evidence of the existence of a precocial bird species' maternal styles. By using an adoption procedure we evaluated how maternal style affected the behaviour of Japanese quail, Coturnix coturnix japonica, chicks, via exclusively nongenomic mechanisms. As well as evidence for the existence of maternal styles in this species, we also found correlations between females' temperaments, maternal styles and their fostered chicks' development. Our findings indicate that maternal styles are key features that help understand nongenomic transmission of behavioural characteristics whose vectors have remained poorly understood.
Motivated behaviors, including sexual experience, activate the mesolimbic dopamine system and produce long-lasting molecular and structural changes in the nucleus accumbens. The transcription factor ΔFosB is hypothesized to partly mediate this experience-dependent plasticity. Previous research in our laboratory has demonstrated that overexpressing ΔFosB in the nucleus accumbens of female Syrian hamsters augments the ability of sexual experience to cause the formation of a conditioned place preference. It is unknown, however, whether ΔFosB-mediated transcription in the nucleus accumbens is required for the behavioral consequences of sexual reward. We therefore used an adeno-associated virus to overexpress ΔJunD, a dominant negative binding partner of ΔFosB that decreases ΔFosB-mediated transcription by competitively heterodimerizing with ΔFosB before binding at promotor regions on target genes, in the nucleus accumbens. We found that overexpression of ΔJunD prevented the formation of a conditioned place preference following repeated sexual experiences. These data, when coupled with our previous findings, suggest that ∆FosB is both necessary and sufficient for behavioral plasticity following sexual experience. Furthermore, these results contribute to an important and growing body of literature demonstrating the necessity of endogenous ΔFosB expression in the nucleus accumbens for adaptive responding to naturally rewarding stimuli.
Sexually naive male mice show robust aggressive behavior toward pups. However, the proportion of male mice exhibiting pup-directed aggression declines after cohabitation with a pregnant female for 2 weeks after mating. Subsequently, on becoming fathers, they show parental behavior toward pups, similar to maternal behavior by mothers. To elucidate the neural mechanisms underlying this behavioral transition, we examined brain regions differentially activated in sexually naive males and fathers after exposure to pups, using c-Fos expression as a neuronal activation marker. We found that, after pup exposure, subsets of neurons along the vomeronasal neural pathway-including the vomeronasal sensory neurons, the accessory olfactory bulb, the posterior medial amygdala, the medioposterior division of the bed nucleus of stria terminalis, and the anterior hypothalamic area-were more strongly activated in sexually naive males than in fathers. Notably, c-Fos induction was not observed in the vomeronasal sensory neurons of fathers after pup exposure. Surgical ablation of the vomeronasal organ in sexually naive males resulted in the abrogation of pup-directed aggression and simultaneous induction of parental behavior. These results suggest that chemical cues evoking pup-directed aggression are received by the vomeronasal sensory neurons and activate the vomeronasal neural pathway in sexually naive male mice but not in fathers. Thus, the downregulation of pup pheromone-induced activation of the vomeronasal system might be important for the behavioral transition from attack to parenting in male mice.
Drugs of abuse induce neuroplasticity in the natural reward pathway, specifically the nucleus accumbens (NAc), thereby causing development and expression of addictive behavior. Recent evidence suggests that natural rewards may cause similar changes in the NAc, suggesting that drugs may activate mechanisms of plasticity shared with natural rewards, and allowing for unique interplay between natural and drug rewards. In this study, we demonstrate that sexual experience in male rats when followed by short or prolonged periods of loss of sex reward causes enhanced amphetamine reward, indicated by sensitized conditioned place preference for low-dose (0.5 mg/kg) amphetamine. Moreover, the onset, but not the longer-term expression, of enhanced amphetamine reward was correlated with a transient increase in dendritic spines in the NAc. Next, a critical role for the transcription factor ΔFosB in sex experience-induced enhanced amphetamine reward and associated increases in dendritic spines on NAc neurons was established using viral vector gene transfer of the dominant-negative binding partner ΔJunD. Moreover, it was demonstrated that sexual experience-induced enhanced drug reward, ΔFosB, and spinogenesis are dependent on mating-induced dopamine D1 receptor activation in the NAc. Pharmacological blockade of D1 receptor, but not D2 receptor, in the NAc during sexual behavior attenuated ΔFosB induction and prevented increased spinogenesis and sensitized amphetamine reward. Together, these findings demonstrate that drugs of abuse and natural reward behaviors act on common molecular and cellular mechanisms of plasticity that control vulnerability to drug addiction, and that this increased vulnerability is mediated by ΔFosB and its downstream transcriptional targets.
During the early postpartum period or following estrogen/progesterone administration, pups elicit maternal behavior accompanied by a robust dopamine (DA) response in the nucleus accumbens (NAC) of female rats (Afonso et al., 2009). To determine whether DA responds to ostensibly "salient" stimuli in the absence of consummatory behaviors, we examined NAC shell DA responses during restricted (stimuli placed in a perforated box), and unrestricted access to pup and food stimuli. Microdialysis samples were collected from female rats that were either cycling and postpartum (Experiment 1), or after ovariectomy and treated with empty and hormone-filled capsules (Experiment 2). Relative to nonprimed controls, hormonally primed females had suppressed basal DA concentrations and facilitated pup-evoked DA responses, regardless of stimulus access condition. In contrast, food-evoked DA responses were unchanged by hormonal priming and were greater when females consumed food compared with distal (restricted) exposure to food. During pup and food restriction conditions, the lack of any "appetitive" behavioral differences, even in pup experienced postpartum females, was surprising. In Experiment 3, we confirmed that postpartum dams allocated time equivalently to restricted pup and food stimuli, even after pup deprivation. This was in sharp contrast to the effects of deprivation during the unrestricted access phase. Together, our data demonstrated that, in hormonally primed females, distal pup cues could evoke DA responses without prior stimulus experience, ongoing maternal (behavioral) responses, or clear evidence of robust pup saliency. The results suggest that NAC DA response reflects a state of responsiveness related to basal DA suppression in the hormonally primed female rat.
Two different procedures were followed to induce maternal behaviour in domestic hens. When chicks were placed under hens during the night, the majority of adults presented maternal behaviour the following morning. When chicks were placed in cages at the beginning of the photophase, maternal responses appeared after a 24 h delay; hens first avoided or were aggressive towards chicks. The results are discussed in terms of hens becoming familiar with auditory, tactile and visual stimuli from chicks.
We investigated the neuroendocrine changes involved in the transition from incubating eggs to brooding of the young in turkeys. Numbers of mesotocin (MT; the avian analog of mammalian oxytocin) immunoreactive (ir) neurons were higher in the nucleus paraventricularis magnocellularis (PVN) and nucleus supraopticus, pars ventralis (SOv) of late stage incubating hens compared to the layers. When incubating and laying hens were presented with poults, all incubating hens displayed brooding behavior. c-fos mRNA expression was found in several brain areas in brooding hens. The majority of c-fos mRNA expression by MT-ir neurons was observed in the PVN and SOv while the majority of c-fos mRNA expression in dopaminergic (DAergic) neurons was observed in the ventral part of the nucleus preopticus medialis (POM). Following intracerebroventricular injection of DA or oxytocin (OT) receptor antagonists, hens incubating eggs were introduced to poults. Over 80% of those injected with vehicle or the D1 DA receptor antagonist brooded poults, while over 80% of those receiving the D2 DA receptor antagonist or the OT receptor antagonist failed to brood the poults. The D2 DA/OT antagonist groups also displayed less c-fos mRNA in the dorsal part of POM and the medial part of the bed nucleus of the stria terminalis (BSTM) areas than did the D1 DA/vehicle groups. These data indicate that numerous brain areas are activated when incubating hens initially transition to poult brooding behavior. They also indicate that DAergic, through its D2 receptor, and MTergic systems may play a role in regulating brooding behaviors in birds.
Rodent paternal models provide unique opportunities to investigate the emergence of affiliative social behavior in mammals. Using biparental and uniparental Peromyscus species (californicus and maniculatus, respectively) we assessed paternal responsiveness by exposing males to biological offspring, unrelated conspecific pups, or familiar brothers following a 24-hour separation. The putative paternal circuit we investigated included brain areas involved in fear/anxiety [cingulate cortex (Cg), medial amygdala (MeA), paraventricular nucleus of the hypothalamus (PVN), and lateral septum (LS)], parental motivation [medial preoptic area (MPOA)], learning/behavioral plasticity (hippocampus), olfaction [pyriform cortex (PC)], and social rewards (nucleus accumbens). Paternal experience in californicus males reduced fos immunoreactivity (ir) in several fear/anxiety areas; additionally, all californicus groups exhibited decreased fos-ir in the PC. Enhanced arginine vasopressin (AVP) and oxytocin (OT)-ir cell bodies and fibers, as well as increased neuronal restructuring in the hippocampus, were also observed in californicus mice. Multidimensional scaling analyses revealed distinct brain activation profiles differentiating californicus biological fathers, pup-exposed virgins, and pup-naïve virgins. Specifically, associations among MPOA fos, CA1 fos, dentate gyrus GFAP, CA2 nestin-, and PVN OT-ir characterized biological fathers; LS fos-, Cg fos-, and AVP-ir characterized pup-exposed virgins, and PC-, PVN-, and MeA fos-ir characterized pup-naïve virgins. Thus, whereas fear/anxiety areas characterized pup-naïve males, neurobiological factors involved in more diverse functions such as learning, motivation, and nurturing responses characterized fatherhood in biparental californicus mice. Less distinct paternal-dependent activation patterns were observed in uniparental maniculatus mice. These data suggest that dual neurobiological circuits, leading to the inhibition of social-dependent anxiety as well as the activation of affiliative responses, characterize the transition from nonpaternal to paternal status in californicus mice.
Quality of mothering relies on the integrity of multiple physiological and behavioral systems and on two maternal factors, one proximal and one distal, that have a great impact on how a mother mothers: postpartum depression and early experiences. To mother appropriately requires the action of systems that regulate sensation, perception, affect, reward, executive function, motor output and learning. When a mother is at risk to engage in less than optimal mothering, such as when she is depressed or has experienced adversity in childhood, the function of many or all of maternal and related systems may be affected. In this paper, we will review what is currently known about the biological basis of mothering, with attention to literature on hormones but with a particular focus on recent advances in the fields of functional neuroimaging. Instead of discussing strictly 'maternal' brain imaging studies, we instead use a systems approach to survey important findings relevant to brain systems integral to and/or strongly related to the mothering experience: (a) social behavior; (b) reward and affect; (c) executive function; and (d) maternal behavior. We find that there are many commonalities in terms of the brain regions identified across these systems and, as we would expect, all are sensitive to the influence of, or function differently in the context of, depression and adverse early experience. It is likely that the similarity and cross-talk between maternal, affect and stress systems, observed behaviorally, hormonally and in the context of brain function, allows for mood disturbance and early adverse experiences to have a significant impact on the quality of mothering and the motivation to mother.
Memory formation is a temporally graded process during which transcription and translation steps are required in the first hours after acquisition. Although persistence is a key characteristic of memory storage, its mechanisms are scarcely characterized. Here, we show that long-lasting but not short-lived inhibitory avoidance long-term memory is associated with a delayed expression of c-Fos in the hippocampus. Importantly, this late wave of c-Fos is necessary for maintenance of inhibitory avoidance long-term storage. Moreover, inhibition of transcription in the dorsal hippocampus 24 h after training hinders persistence but not formation of long-term storage. These findings indicate that a delayed phase of transcription is essential for maintenance of a hippocampus-dependent memory trace. Our results support the hypothesis that recurrent rounds of consolidation-like events take place late after learning in the dorsal hippocampus to maintain memories.
Beyond the genetic links between mother and young, prenatal effects experienced by offspring can modulate their mother’s behaviour and stress. Here we investigated the consequences of stress-induced prenatal maternal effects on quail chicks’ behaviour and maternal behaviour. We evaluated how adoptive quail mothers (unstressed) raised chicks of females that had either been stressed (PS) or were non-stressed (NPS) during laying. We demonstrated previously that our social stress procedure during laying increases levels of egg yolk steroid and chicks’ emotional reactivity during the postnatal period. We found that, compared to NPS mothers, PS mothers remained closer to their chicks, were aggressed and neglected them less, emitted more maternal vocalisations and called their chicks more when they were separated. Moreover, PS chicks made more requests on their mother. Our results show that mothers responded to chicks’ behavioural changes caused by prenatal stress by adapting their maternal behaviour. As exemplified here, for the first time in birds, prenatal environment can affect postnatal maternal behaviour by changing their offspring’s behaviour.
Maternal behavior develops differently depending on characteristics of the individual, such as age or emotional reactivity. Social motivation, defined as the propensity to establish social contact, has been little studied in relation to maternal behavior in birds. In addition, the transition to motherhood is a time of plasticity in the brain of the new mother in mammals. However, it remains to be determined how maternal brain plasticity is affected in avian species. The present study investigated how a mother's social motivation alters maternal behavior and brain plasticity of the Japanese quail (Coturnix japonica). Adult females from lines selected for high and low social motivation were exposed to chicks for 11 days. After maternal care testing, and at matched time points in controls, the brains of females were perfused for assessing immunoreactivity staining of doublecortin, a marker of neurogenesis, in the subventricular zone (SVZ), a neurogenic niche. Our results showed that high socially motivated female quail spent significantly less time in maternal behaviour when exposed to chicks compared to low socially motivated females. Moreover, the high social motivated females warmed chicks with less covering postures and were more rejecting of chicks. Interestingly, the plasticity indicators in the SVZ did not differ between low and high social motivated females and were not associated with differences in maternal caregiving when using doublecortin‐immunoreactive staining. Thus, high social motivation in this avian species does not favour maternal behavior and this level of motivation to mother is not related to changes in neuroplasticity in the SVZ of the female quail.
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The pituitary neuropeptide oxytocin promotes social behavior, and is a potential adjunct therapy for social deficits in schizophrenia and autism. Oxytocin may mediate pro-social effects by modulating monoamine release in limbic and cortical areas, which was investigated herein using in vivo microdialysis, after establishing a dose that did not produce accompanying sedative or thermoregulatory effects that could concomitantly influence behavior. The effects of oxytocin (0.03-0.3 mg/kg subcutaneous) on locomotor activity, core body temperature, and social behavior (social interaction and ultrasonic vocalizations) were examined in adult male Lister-hooded rats, using selective antagonists to determine the role of oxytocin and vasopressin V1a receptors. Dopamine and serotonin efflux in the prefrontal cortex and nucleus accumbens of conscious rats were assessed using microdialysis. 0.3 mg/kg oxytocin modestly reduced activity and caused hypothermia but only the latter was attenuated by the V1a receptor antagonist, SR49059 (1 mg/kg intraperitoneal). Oxytocin at 0.1 mg/kg, which did not alter activity and had little effect on temperature, significantly attenuated phencyclidine-induced hyperactivity and increased social interaction between unfamiliar rats without altering the number or pattern of ultrasonic vocalizations. In the same rats, oxytocin (0.1 mg/kg) selectively elevated dopamine overflow in the nucleus accumbens, but not prefrontal cortex, without influencing serotonin efflux. Systemic oxytocin administration attenuated phencyclidine-induced hyperactivity and increased pro-social behavior without decreasing core body temperature and selectively enhanced nucleus accumbens dopamine release, consistent with activation of mesocorticolimbic circuits regulating associative/reward behavior being involved. This highlights the therapeutic potential of oxytocin to treat social behavioral deficits seen in psychiatric disorders such as schizophrenia.
Approach/avoid model is used to analyze the neural regulation of maternal behavior in the laboratory rat. This model proposes that the medial preoptic area (mPOA) and bed nucleus of stria terminalis (BNST) are brain regions involved in facilitating mechanisms. By contrast, anterior hypothalamic nucleus (AHN), ventromedial hypothalamic nucleus (VMH), and periaqueductal gray participate in the inhibiting mechanisms of neural regulation of maternal behavior. We hypothesized that there are also facilitating and inhibiting mechanisms in the neural regulation of paternal behavior. Here, we determined which neural areas are activated during paternal and aversive interactions with pups in the Mongolian gerbils (Meriones unguiculatus). By testing paternal behavior, we selected 40 males aggressive toward pups and 20 paternal males. These males were organized into six groups of 10 animals in each group: aggressive males that interacted with pups (AGG-pups) or candy (AGG-candy), paternal males that interacted with pups (PAT-pups) or candy (PAT-candy), and males with testosterone (T)-induced paternal behavior that interacted with pups (IPAT-pups) or candy (IPAT-candy). After interacting with pups or candy, the brains were extracted and analyzed for immunoreactivity (ir) with c-fos. Males that interacted with pups had significantly higher c-fos-ir in the mPOA/BNST than males that interacted with candy. Males that displayed aggression had significantly higher c-fos-ir in the AHN, VMH, and periaqueductal gray than aggressive males that interacted with candy. These results suggest that in the neural regulation of paternal behavior in the Mongolian gerbil underlie positive and negative mechanisms as occurs in maternal behavior.
Maternal behaviors are essential for the survival of the young. Previous studies implicated the medial preoptic area (MPOA) as an important region for maternal behaviors, but details of the maternal circuit remain incompletely understood. Here we identify estrogen receptor alpha (Esr1)-expressing cells in the MPOA as key mediators of pup approach and retrieval. Reversible inactivation of MPOAEsr1+cells impairs those behaviors, whereas optogenetic activation induces immediate pup retrieval. In vivo recordings demonstrate preferential activation of MPOAEsr1+cells during maternal behaviors and changes in MPOA cell responses across reproductive states. Furthermore, channelrhodopsin-assisted circuit mapping reveals a strong inhibitory projection from MPOAEsr1+cells to ventral tegmental area (VTA) non-dopaminergic cells. Pathway-specific manipulations reveal that this projection is essential for driving pup approach and retrieval and that VTA dopaminergic cells are reliably activated during those behaviors. Altogether, this study provides new insight into the neural circuit that generates maternal behaviors.
Behaviour of young domestic chicks when isolated from conspecifics is influenced by two conflicting drives: fear of potential predator and craving for company. The nucleus accumbens (Ac) has been suggested to influence social behaviour, as well as motivation in goal directed tasks. In the present study, the Ac of one-day-old domestic chicks was lesioned bilaterally, using radiofrequency method. Open field behaviour before and after presenting a silhouette of a bird of prey was recorded, followed by a behavioural test to measure group-size preference and social motivation of chicks. Ac lesioned individuals emitted more distress calls and ambulated more in the open field test, however they reacted to the predatory stimulus very similarly to control chicks: their vocalization was reduced and the intergroup difference in motor activity also disappeared. There was no difference between the lesioned and control chicks in the latency to approach their conspecifics in the social motivation test, and both groups chose the larger flock (8) of conspecifics over the smaller one (3). Concerning the role of Ac in social behaviour, a difference between lesioned and sham birds was evident here only in the absence of detectable stimulus (predator or conspecifics). These findings may reflect either decreased fear of exposure to predators, or increased craving for conspecifics, suggesting that the likely function of Ac is to modulate goal-driven, including socially driven, behaviours, especially when the direct stimulus representing the goal is absent. This is in harmony with the known promotion of impulsiveness by Ac lesions. This article is protected by copyright. All rights reserved.
Maternal interactions with young occupy most of the reproductive period for female mammals and are absolutely essential for offspring survival and development. The hormonal, sensory, reward-related, emotional, cognitive and neurobiological regulators of maternal caregiving behaviors have been well studied in numerous subprimate mammalian species, and some of the importance of this body of work is thought to be its relevance for understanding similar controls in humans. We here review many of the important biopsychological influences on maternal behaviors in the two best studied non-human animals, laboratory rats and sheep, and directly examine how the conceptual framework established by some of the major discoveries in these animal "models" do or do not hold for our understanding of human mothering. We also explore some of the limits for extrapolating from non-human animals to humans. We conclude that there are many similarities between non-human and human mothers in the biological and psychological factors influencing their early maternal behavior and that many of the differences are due to species-characteristic features related to the role of hormones, the relative importance of each sensory system, flexibility in what behaviors are exhibited, the presence or absence of language, and the complexity of cortical function influencing the behavior.
Copyright © 2015. Published by Elsevier Inc.
Maternal care is indispensable for the survival of mammalian offspring. Although virgin female mice avoid pups, they actively display maternal behavior after parturition. To determine which brain regions are involved in the qualitative differences observed in the responses of virgin and lactating females to pups, we compared the expression of c-Fos, which is a marker of neuronal activation, in brain regions involved in regulating maternal behavior. Pup presentation increased the number of c-Fos-positive cells in both the ventrotegmental area (VTA) and nucleus accumbens to a greater extent in lactating females than in virgin females. The bed nucleus of striaterminalis (BNST), which innervates VTA neurons to regulate both aversive and rewarding responses, showed increased number of c-Fos-positive cells following pup presentation in virgin females, butnotin lactating females. On the other hand, the number of c-Fos-positive cells in the medial preoptic area (MPOA) increased in both virgin and lactating females. The number of c-Fos-positive cells in lactating females not presented with pups was high and similar to that in virgin females presented with pups. Moreover, c-Fos-positive GABAergicneurons projecting from the MPOA to the BNST was confirmed using a retrograde tracer Fluorogold in lactating females. Our results indicate that constitutive GABAergic modulation projecting from the MPOA may suppress the activity of BNST neurons and prevent avoidance responses to pups in lactating females.
Copyright © 2015. Published by Elsevier Ireland Ltd.
Nitric oxide (NO) acts in the medial preoptic area (mPOA) of the hypothalamus to facilitate the expression of male sexual behavior and has also been widely implicated in mechanisms of experience, learning, and memory. Using immunohistochemistry for Fos, as a marker for neural activity, and nitric oxide synthase (NOS), the enzyme that catalyzes the production of nitric oxide (NO), we examined whether sexual activity and sexual experience influence Fos co-expression in NOS-containing neurons in the mPOA of male rats. Consistent with previous findings, results indicate that mating increased activity in the mPOA, and that sexual experience facilitated the expression of sexual behaviors, together with increased mating-induced Fos and NOS in the mPOA. Results also indicate that mating increased co-expression of Fos in NOS-containing neurons, and that this increase was highest in animals undergoing their first sexual encounter, indicating that initial sexual experience increases NO production in the mPOA of male rats.
Effects of acute and chronic psychological stress in the brain of domestic avian species have not been extensively studied. Experiments were performed using restraint stress to determine groups of neurons activated in the septum and diencephalon of chickens. Using FOS immunoreactivity six brain structures were shown activated by acute stress including: the lateral hypothalamic area (LHy), ventrolateral thalamic nucleus (VLT), lateral septum (LS), lateral bed nucleus of the stria terminalis (BSTL), nucleus of the hippocampal commissure (NHpC) and the core region of the paraventricular nucleus (PVNc). Additionally, the LHy and PVNc showed increased FOS immunoreactive (-ir) cells in the birds chronically stressed when compared to controls. In contrast, the NHpC showed decreased FOS-ir cells following the 10 day chronic stress imposed.. Thereafter, restraint stress experiments were performed to identify activated arginine vasotocin (AVT) neurons (parvocellular or magnocellular) using immunocytochemistry. Of the six FOS activated structures, the PVN was known to contain distinct size groups of AVT-ir neurons, parvocellular (small), medium sized and magnocellular (large). Using dual immunostaining (AVT/FOS), AVT-ir parvocellular neurons in the PVNc were found activated in both acute and chronic stress. To determine whether these AVT-ir parvocellular neurons are co-localized with corticotropin releasing hormone (CRH), an attempt was made to visualize CRH-ir neurons using colchicine. Although AVT-ir and CRH-ir parvocellular neurons occur in the PVNc, only a few neurons were shown co-localized with AVT and CRH after acute restraint stress. Results of this study suggest that the NHpC, LS, VLT, BSTL, LHy and AVT-ir parvocellular neurons in the PVNc are associated with psychological stress in birds.
This article summarizes research on the brain circuits underlying maternal responsiveness. The research shows how a female mammal's physiological state primes and activates neural and neurochemical mechanisms that promote maternal responsiveness. A dysregulation of such mechanisms would lead to inadequate maternal behavior. Neural models are described to show how hormones and oxytocin might cause a functional rewiring of neural circuits so that infant stimuli that initially provoke antisocial defensive responses can come to evoke prosocial acceptance responses. Similarly, genetic, experiential, and cognitive factors might also influence maternal behavior by affecting the operation of the critical neural circuits.
Environmental stimulation results in an increased expression of transcription factors called immediate early genes (IEGs) in specific neuronal populations. In male Japanese quail, copulation with a female increases the expression of the IEGs zenk and c-fos in the medial pre-optic nucleus (POM), a key nucleus controlling male sexual behavior. The functional significance of this increased IEG expression that follows performance of copulatory behavior is unknown. We addressed this question by repeatedly quantifying the performance of appetitive (learned social proximity response) and consummatory (actual copulation) sexual behavior in castrated, testosterone-treated males that received daily intra-cerebroventricular injection of an antisense oligodeoxynucleotide targeting c-fos or control vehicle. Daily antisense injections significantly inhibited the expression of copulatory behavior as well as the acquisition of the learned social proximity response. A strong reduction of the proximity response was still observed in antisense-treated birds that copulated with a female, ruling out the indirect effect of the absence of interactions with females on the learning process. After a 2-day interruption of behavioral testing but not of antisense injections, birds were submitted to a final copulatory test that confirmed the behavioral inhibition in antisense-injected birds. Brains were collected at 90 min after the behavioral testing for quantification of c-fos-immunoreactive cells. A significant reduction of the number of c-fos-positive cells in the POM but not in other brain regions was observed following antisense injection. Taken together, the data suggest that c-fos expression in the POM modulates copulatory behavior and sexual learning in male quail.
Most studies regarding altered gene expression after learning are performed using multi-trial tasks, which do not allow a clear discrimination of memory acquisition, consolidation and retrieval. We screened for candidate memory-modulated genes in the hippocampus at 3 and 24 h after one-trial inhibitory avoidance (IA) training, using a cDNA array containing 1176 genes. While 33 genes were modulated by training (respect to shocked-only animals), most of them were upregulated (27 genes) and only 6 were downregulated. To confirm and extend these findings, we performed RT-PCRs and analyzed differences in protein levels in rat hippocampus using immunoblot assays. We found several proteins upregulated 24 h after training: extracellular signal-regulated kinase ERK2, Ca2+/calmodulin-dependent protein kinase II alpha (CaMKIIα), Syntaxin 1a, c-fos and Homer 1a. The total level of none of these proteins were found to be altered when measured 3-h post-training. Several of the mRNAs corresponding to the upregulated proteins were changed at 3 h but not 24 h. Additionally, a number of other candidates were identified for the first time as modulated by learning. The results presented here suggest that single-trial tasks can expose previously unseen differences in dynamic regulation of gene expression after behavioral manipulations, both at the transcriptional and translational levels, and reveal a diversity of gene products modulated by this task, allowing deeper understanding of the molecular basis of memory formation.
The aim of this study was to determine whether mothers' fear of human could influence the way young domestic Japanese quail respond to human. The first step was to obtain a set of adoptive mothers habituated-to-human (H mothers) and a set of adoptive mothers non-habituated-to-human (NH mothers). A set of 6-month-old adult females was handling daily for 15 successive days whereas another set of 6-month-old adult females received no visual or physical contact with human during the same period. We then obtained two sets of adoptive mothers non-divergent in tonic immobility (TI) duration but divergent by the amount of "fear" behaviour expressed towards human (human observer test, cage-plus-experimenter test). Then, we compared a set of young raised by H mothers to a set of young raised by NH mothers. Observations and tests were carried out both during the brooding period (between 5 and 12 days of age) and after separation from mothers (between 13 and 90 days of age). Our results revealed that young raised by H mothers were less fearful towards a static human (cage-plus-experimenter test, hand-on-home-cage-door-test) as well as towards a moving human (human observer test and capture test) than young raised by NH mothers. Nevertheless, as was found between the two sets of adoptive mothers, no clear differences were found between the two sets of young concerning general emotional reactivity (tonic immobility test, open field test and hole-in-the-wall test). These results reveal that young bird's emotional reactivity to human could be modulated by the mother and that this maternal influence remains detectable well after the end of maternal contact. (C) 2004 Elsevier B.V. All rights reserved.
In rodents, previous findings indicate critical involvement of the medial preoptic area (MPOA) in the neural control of maternal behavior. However, the specification of the particular MPOA subregions involved in maternal behavior and the identification of the neurochemical phenotype(s) of the essential neurons demands additional study. Therefore, we investigated the chemical neuroanatomy of the essential MPOA subregion for maternal behavior in C57BL/6J female mice. Using the oxytocinergic neurons in the dorsal MPOA as a primary regional marker, we first assessed the distribution of c-Fos expressing neurons in the MPOA during maternal behavior using immunohistochemistry. Results showed that non-oxytocinergic neurons in the dorsal and ventral MPOA prominently expressed c-Fos during maternal behavior. Then using excitotoxic lesion studies, we determined the specific MPOA area that is necessary for maternal behavior. Bilateral lesions of the central MPOA, where c-Fos was expressed only moderately, effectively disrupted maternal behavior, although lesions to the dorsal and ventral MPOA regions were ineffective. These centrally lesioned females were highly infanticidal irrespective of their previous maternal experience. Neurochemical investigations showed that more than 75% of the c-Fos-expressing neurons in central MPOA were GABAergic. Many of them also expressed galanin, neurotensin, and/or tachykinin2 mRNAs. Finally, the central MPOA was populated by numerous glutamatergic neurons, although only a small percentage of these neurons colocalized with c-Fos. To conclude, the central MPOA is the indispensable subregion for mouse maternal behavior, and GABAergic and/or peptidergic neurons in this area were transcriptionally activated during maternal behavior. J. Comp. Neurol., 2012. © 2012 Wiley Periodicals, Inc.
Juvenile rats can exhibit maternal behavior after being exposed continuously to rat pups, a process called sensitization. Maternal behavior in juveniles is robust and is similar to adult maternal behavior (Mayer and Rosenblatt [1979] Dev. Psychobiol. 12:407–424; Gray and Chesley [684] J. Comp. Psychol. 98:91–99). In this study, immunocytochemical detection of the protein products of two immediate-early genes, c-fos and fosB, was used as a tool to identify forebrain neuronal populations involved in the maternal behavior of 27-day-old juvenile rats compared with 60-day-old adults. To sensitize them, rats were exposed continuously to foster pups. Once they were maternal, they were isolated from pups overnight, reexposed to pups for 2 hours, and then killed. Nonmaternal control animals also were isolated overnight and were either reexposed to pups for 2 hours or kept isolated from pups before killing. The lateral habenula (LH) was the only area in which both maternal juveniles and maternal adults had more c-Fos-immunoreactive (-Ir) neurons compared with controls. In maternal adults, the number of neurons that expressed c-Fos and FosB immunoreactivity increased in the medial preoptic area (MPO) and the ventral bed nucleus of the stria terminalis (BSTv), whereas the dorsal bed nucleus of the stria terminalis (BSTd) and the medial and cortical nuclei of the amygdala (MEA and COA, respectively) had increases only in the number of neurons that expressed c-Fos immunoreactivity. In contrast, juveniles, whether or not they were maternal, had the same number of c-Fos-IR and FosB-Ir neurons in all these areas. The adult-like increase in the number of c-Fos-Ir neurons found in maternal juveniles suggests that the juvenile LH participates in the neural circuit that supports maternal behavior in an adult-like manner. The lack of c-fos or fosB induction in the MPO, BSTv, BSTd, COA, or MEA of maternal juveniles compared with maternal adults may reflect the immaturity of these brain regions in juvenile rats. Exactly what this immaturity consists of and when the responses of these regions become adult-like remain to be determined. J. Comp. Neurol. 416:45–78, 2000. © 2000 Wiley-Liss, Inc.
Maternal behavior in rats undergoes considerable plasticity in parallel to the developmental stage of the pups, resulting in distinct patterns of maternal behavior and care at different postpartum time points. The medial preoptic area (mPOA) of the hypothalamus is one critical neural substrate underlying the onset and early expression of maternal behavior in rats but little is known about its specific functional role in the evolving expression of maternal behavior across the postpartum period. The present study uses a reversible local neural inactivation method to examine the role of the mPOA in the regulation of maternal behavior throughout the postpartum period, particularly extending into the late postpartum, a little examined period. This approach avoids the compensatory plasticity in CNS that occurs after permanent lesions, and allows the repeated testing of same individuals. Early (PPD7–8) and late (PPD13–14) postpartum maternal behavior was evaluated in female rats following infusions of bupivacaine or vehicle into the mPOA or into control areas. As expected, mPOA inactivation severely but transiently disrupted early postpartum maternal behavior whereas infusion of vehicle or inactivation of adjacent control sites did not. Later in the postpartum period, however, transient mPOA inactivation facilitated the expression of maternal behaviors, highly contrasting the behavioral expression levels characteristic of late postpartum. Results strongly demonstrate that the mPOA is differentially engaged throughout postpartum in orchestrating appropriate maternal responses with the developmental stage of the pups.
The present study investigated hormonal mediation of maternal behavior and accumbal dopamine (DA) responses to pup-stimuli, as measured in microdialysis samples collected from the nucleus accumbens shell of female rats in non-homecage environment. In Experiment 1, samples were collected before and after continuous homecage pup experience from either intact postpartum or cycling females. In Experiment 2, samples were collected before and after responding maternally in homecage from ovariectomized females given either parturient-like hormone or sham treatments. After baseline sample collection in the dialysis chamber, pup and food stimuli were individually presented to females. Upon sampling completion, all animals were placed back into their homecage with donor pups for several days, and then the sample collection procedure was repeated. Prior to stimulus presentation, postpartum and hormone-treated females had decreased basal DA release compared to their controls. In response to pup stimuli, only postpartum and hormone-treated females had increased DA release compared to basal release (both sampling days). In response to food stimuli, all females had increased DA responses from basal; although there were group differences on the initial day of sampling. Findings suggest that hormones associated with inducing maternal behavior in the postpartum rat play a significant role in modifying accumbal dopaminergic responses on first exposure to pup stimuli in the rat. However, the postpartum experience provides further modifications to this brain region to promote DA responses to pup stimuli.
In a minority of mammalian species, including humans, fathers play a significant role in infant care. Compared to maternal behavior, the neural and hormonal bases of paternal care are poorly understood. We analyzed behavioral, neuronal and neuropeptide responses towards unfamiliar pups in biparental California mice, comparing males housed with another male (“virgin males”) or with a female before (“paired males”) or after (“new fathers”) the birth of their first litter. New fathers approached pups more rapidly and spent more time engaging in paternal behavior than virgin males. In each cage housing two virgin males, one was spontaneously paternal and one was not. New fathers and paired males spent more time sniffing and touching a wire mesh ball containing a newborn pup than virgin males. Only new fathers showed significantly increased Fos-like immunoreactivity in the medial preoptic nucleus (MPO) following exposure to a pup-containing ball, as compared to an empty ball. Moreover, Fos-LIR in the bed nucleus of the stria terminalis (STMV and STMPM) and caudal dorsal raphe nucleus (DRC) was increased in new fathers, independent of test condition. No differences were found among the groups in Fos-LIR in oxytocinergic or vasopressinergic neurons. These results suggest that sexual and paternal experiences facilitate paternal behavior, but other cues play a role as well. Paternal experience increases Fos-LIR induced by distal pup cues in the MPO, but not in oxytocin and vasopressin neurons. Fatherhood also appears to alter neurotransmission in the BNST and DRC, regions implicated in emotionality and stress-responsiveness.
All animals evaluate the salience of external stimuli and integrate them with internal physiological information into adaptive behavior. Natural and sexual selection impinge on these processes, yet our understanding of behavioral decision-making mechanisms and their evolution is still very limited. Insights from mammals indicate that two neural circuits are of crucial importance in this context: the social behavior network and the mesolimbic reward system. Here we review evidence from neurochemical, tract-tracing, developmental, and functional lesion/stimulation studies that delineates homology relationships for most of the nodes of these two circuits across the five major vertebrate lineages: mammals, birds, reptiles, amphibians, and teleost fish. We provide for the first time a comprehensive comparative analysis of the two neural circuits and conclude that they were already present in early vertebrates. We also propose that these circuits form a larger social decision-making (SDM) network that regulates adaptive behavior. Our synthesis thus provides an important foundation for understanding the evolution of the neural mechanisms underlying reward processing and behavioral regulation.
Interacting parenting thoughts and behaviors, supported by key brain circuits, critically shape human infants' current and future behavior. Indeed, the parent-infant relationship provides infants with their first social environment, forming templates for what they can expect from others, how to interact with them and ultimately how they go on to themselves to be parents. This review concentrates on magnetic resonance imaging experiments of the human parent brain, which link brain physiology with parental thoughts and behaviors. After reviewing brain imaging techniques, certain social cognitive and affective concepts are reviewed, including empathy and trust-likely critical to parenting. Following that is a thorough study-by-study review of the state-of-the-art with respect to human neuroimaging studies of the parental brain-from parent brain responses to salient infant stimuli, including emotionally charged baby cries and brief visual stimuli to the latest structural brain studies. Taken together, this research suggests that networks of highly conserved hypothalamic-midbrain-limbic-paralimbic-cortical circuits act in concert to support parental brain responses to infants, including circuits for limbic emotion response and regulation. Thus, a model is presented in which infant stimuli activate sensory analysis brain regions, affect corticolimbic limbic circuits that regulate emotional response, motivation and reward related to their infant, ultimately organizing parenting impulses, thoughts and emotions into coordinated behaviors as a map for future studies. Finally, future directions towards integrated understanding of the brain basis of human parenting are outlined with profound implications for understanding and contributing to long term parent and infant mental health.
The medial preoptic area (MPOA) of the hypothalamus regulates maternal behavior, male sexual behavior, and female sexual behavior. Functional neuroanatomical evidence indicates that the appetitive aspects of maternal behavior are regulated through MPOA interactions with the mesolimbic dopamine (DA) system; a major focus of this review is to explore whether or not the MPOA participates in the appetitive aspects of sexual behavior via its interaction with the mesolimbic DA system. A second focus of this review is to examine the extent to which estradiol interactions with DA within this circuit regulate all three reproductive behaviors. One mechanism through which estradiol activates male sexual behavior is through the potentiation of DA activity in the MPOA. In the hypothalamus, estradiol has also been found to act in concert with DA, through the activation of similar intracellular signaling pathways, in order to stimulate female sexual behavior. Finally, recent evidence suggests that some effects of estradiol are mediated by direct action of estradiol on the mesolimbic DA system.
Female rats with maternal experience display a shorter onset of maternal responsiveness compared to those with no prior experience. This phenomenon called 'maternal memory' is critically dependent on the nucleus accumbens (NA) shell. We hypothesized that activation of OT receptors in the NA shell facilitates maternal memory. In Experiment 1, postpartum female rats given 1 hour of maternal experience were infused following the experience with either a high or low dose of an OT antagonist into the NA shell and tested for maternal behavior after a 10-day pup isolation period. Females receiving a high dose of the antagonist showed a significantly longer latency to exhibit full maternal behavior after the pup isolation period compared to females that received vehicle or a high dose of antagonist in a control region. In Experiment 2, postpartum female rats were infused with either a high or low dose of OT into the NA shell after a 15-minute maternal experience and tested for maternal behavior after a 10-day pup isolation period. There were no significant differences between the females infused with OT and females treated with a vehicle infused into the NA shell or with OT infused into the control region. One possible reason for a lack of facilitation is a floor effect, since females in the control groups displayed a rapid maternal response after the pup isolation period. These findings suggest that OT receptors, likely in combination with other neurotransmitters, in the NA shell play a role in the consolidation of maternal memory.