Functional, anatomical, and neurochemical differentiation of medial preoptic area subregions in relation to maternal behavior in the mouse

Yousuke Tsuneoka · Teppo Maruyama · Sachine Yoshida · Katsuhiko Nishimori · Tadafumi Kato · Michael Numan +1 more

206 citations0/0 files storedThe Journal of Comparative Neurology

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Neuroendocrine regulation and behavior Neuropeptides and Animal Physiology Neurogenesis and neuroplasticity mechanisms

Abstract

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.

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References

1979Induction of maternal behavior in virgin rats after intracerebroventricular administration of oxytocin 1996Oxytocin is required for nursing but is not essential for parturition or reproductive behavior.1967Nonhormonal Basis of Maternal Behavior in the Rat 1982Natural selection and social behavior 2003The Neurobiology of Parental Behavior 2009Evidence That Oxytocin Exerts Anxiolytic Effects via Oxytocin Receptor Expressed in Serotonergic Neurons in Mice 1981Immunohistochemical analysis of magnocellular elements in rat hypothalamus: Distribution and numbers of cells containing neurophysin, oxytocin, and vasopressin 1994Oxytocin activates the postpartum onset of rat maternal behavior in the ventral tegmental and medial preoptic areas.

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2013Behavioral Transition from Attack to Parenting in Male Mice: A Crucial Role of the Vomeronasal System 2017Prolactin action in the medial preoptic area is necessary for postpartum maternal nursing behavior 2016The neural circuits of mating and fighting in male mice 2014The role of oxytocin in male and female reproductive behavior

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