Current Models and Future Directions for Understanding the Neural Circuitries of Maternal Behaviors in Rodents

Gammie, Stephen C.

doi:10.1177/1534582305281086

Cited by 90 publications

(92 citation statements)

References 162 publications

(146 reference statements)

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“…In contrast to the inhibitory function of the MeA (14-16), our work illustrates the positive involvement of the BLA. Therefore, the maternal deficit in the stathmin Ϫ/Ϫ mice may be different from that in other mutant mice described so far (14,16,26). Also, to our knowledge, the rescue experiment using pup pre-exposure has not been described before.…”

Section: Discussionmentioning

confidence: 93%

Stathmin reveals dissociable roles of the basolateral amygdala in parental and social behaviors

Martel

Nishi

Shumyatsky

2008

Proc. Natl. Acad. Sci. U.S.A.

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Innate parental behaviors and adult social interactions are essential for survival of the individual along with the species as a whole. Because these behaviors require threat assessment of the environment, it is plausible that they are regulated by the amygdalaassociated neural circuitry of fear. However, the amygdala is not a single anatomic and functional unit, and nuclei of the amygdala have multiple inter-and intra-connections. This poses a question as to the exact role of different amygdala nuclei in these behaviors and the mechanisms involved. The basolateral complex of the amygdala nuclei (BLA) is particularly interesting in this regard: although the BLA role in forming memories for learned fear is established, the BLA role in innate behaviors is not well understood. We recently demonstrated that mice without an inhibitor of microtubules, stathmin, a gene enriched in BLA-associated circuitry, have deficiency in innate and learned fear. Here we show that the deficiency in fear processing in stathmin ؊/؊ females leads to improper threat assessment, which in turn affects innate parental care and adult social interactions. Profound deficiency is observed in maternal behavior of stathmin ؊/؊ females: they lack motivation for retrieving pups and are unable to choose a safe location for nest-building. Remarkably, stathmin ؊/؊ females have an enhancement in social interactions. BLA lesions in WT mice produce similar effects in maternal and social behaviors, confirming vital BLA participation. The findings implicate stathmin as the critical molecular component linking the BLA-associated neural circuitry with innate parental behaviors and adult social interactions.amygdala-enriched genes ͉ maternal behavior ͉ fear ͉ threat ͉ pup retrieval A mong Niko Tinbergen's four ''whys,'' representing a framework for understanding animal behavior, the third why refers to the survival value of a behavior (1). As such, a proper threat assessment is crucial in guiding animal and human activities (2, 3). Danger detection is critically dependent on the amygdala (4) and its many nuclei have various neural connections throughout the brain (5-7). Recent work provides clear evidence that amygdala nuclei have different roles in fear-related and reward-related learned behaviors (8-12). Specifically, the basolateral complex of the amygdala nuclei (throughout the article we refer to the lateral, or LA, and basal, or BA, nuclei as the basolateral complex, or BLA) is thought to be the major area of the brain involved in learned fear. However, little is known about the role of the BLA in other behaviors where danger assessment is essential. Unraveling the molecular, cellular, and anatomic mechanisms underlying the relationship between the BLA-associated circuitry and behaviors involving threat assessment may help to better understand behavioral choices in animals and humans.Here we examine the role of the BLA in two behaviors vital for individual safety and species survival: affiliative maternal care and adult social interactions. During mate...

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Section: Discussionmentioning

confidence: 93%

Stathmin reveals dissociable roles of the basolateral amygdala in parental and social behaviors

Martel

Nishi

Shumyatsky

2008

Proc. Natl. Acad. Sci. U.S.A.

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“…Other studies, using expression of the c-fos gene, confirmed the importance of the mpoa, as well as other structures implicated in the activation and inhibition of maternal behavior (e.g., [108,112]). A recent review [29] has provided more detail regarding which of the various components associated with maternal behavior in rodents can be assigned to specific neural circuits. However, none of the studies specifically identified the circuitry involved in detecting and discriminating infant cries, or the circuitry underlying the activation of caregiver responses to the cries.…”

Section: The Neural Circuitry Underlying Cry Perceptionmentioning

confidence: 99%

Neural circuits underlying crying and cry responding in mammals

Newman

2007

Behavioural Brain Research

180

132

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Crying is a universal vocalization in human infants, as well as in the infants of other mammals. Little is known about the neural structures underlying cry production, or the circuitry that mediates a caregiver's response to cry sounds. In this review, the specific structures known or suspected to be involved in this circuit are identified, along with neurochemical systems and hormones for which evidence suggests a role in responding to infants and infant cries. In addition, evidence that crying elicits parental responses in different mammals is presented. An argument is made for including 'crying' as a functional category in the vocal repertoire of all mammalian infants (and the adults of some species). The prevailing neural model for crying production considers forebrain structures to be dispensable. However, evidence for the anterior cingulate gyrus in cry production, and this structure along with the amygdala and some other forebrain areas in responding to cries is presented.

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“…Maternal aggressive (MA) behavior in lactating rats has been described as a subset of maternal behaviors related to protecting offspring from intruders into the nesting environment (Numan 1994;Gammie 2005). MA is found in most mammals and has been characterized as an offensive/aggressive series of actions and postures including direct attacks on an intruder thought to help ensure offspring survival (Numan 1994).…”

Section: Introductionmentioning

confidence: 99%

Intergenerational effects of cocaine on maternal aggressive behavior and brain oxytocin in rat dams

McMurray

Joyner

Middleton

et al. 2008

Stress

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Gestational cocaine treatment results in significantly increased maternal aggression towards an intruder by postpartum day six, while acute postpartum treatment dose dependently decreases maternal aggressive (MA) behavior. Both increased and decreased aggression in the cocainetreated dams are correlated with either decreased or increased levels of oxytocin in the amygdala, respectively. The current study was an effort to determine whether the effect of gestational cocaine on maternal aggression is transient or would continue into the postpartum period; whether an intermittent cocaine treatment regimen, which incorporates gestational and postpartum intermittent cocaine treatment, would differ from chronic daily gestational treatment; and finally, whether next generation female offspring of cocaine-treated or control dams would have altered MA behavior and oxytocin system changes attributable to either prenatal drug exposure, rearing condition or both. We now report no increase in maternal aggression following chronic gestational treatment and significantly lower levels of aggression in intermittently treated dams on postpartum day eight, with no significant effects in either group on postpartum day 12. Young adult female offspring of the cocaine-treated and control dams, who reared their own natural litters and were tested on postpartum day eight for maternal aggression, had higher levels of maternal aggression towards an intruder attributable to both prenatal cocaine exposure and rearing condition. Higher aggression in cocaine-reared next generation dams was associated with lower levels of oxytocin in the amygdala. Intergenerational effects of cocaine were apparent with respect to aggression and oxytocin system changes.

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Current Models and Future Directions for Understanding the Neural Circuitries of Maternal Behaviors in Rodents

Cited by 90 publications

References 162 publications

Stathmin reveals dissociable roles of the basolateral amygdala in parental and social behaviors

Stathmin reveals dissociable roles of the basolateral amygdala in parental and social behaviors

Neural circuits underlying crying and cry responding in mammals

Intergenerational effects of cocaine on maternal aggressive behavior and brain oxytocin in rat dams

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