Amygdalohippocampal Area Neurons That Project to the Preoptic Area Mediate Infant-Directed Attack in Male Mice

Male animals may show alternative behaviors toward infants: attack or parenting. These behaviors are triggered by pup stimuli under the influence of the internal state, including the hormonal environment and/or social experiences. Converging data suggest that the medial preoptic area (MPOA) contribu...

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Bibliographic Details
Published in:The Journal of neuroscience 2020-05, Vol.40 (20), p.3981-3994
Main Authors: Sato, Keiichiro, Hamasaki, Yumi, Fukui, Kiyoshiro, Ito, Kazuki, Miyamichi, Kazunari, Minami, Masabumi, Amano, Taiju
Format: Article
Language:English
Subjects:
Activation
Aggression - physiology
Aggressive behavior
Amygdala - cytology
Amygdala - physiology
Animal behavior
Animals
Behavior
Brain Mapping
Cortex (olfactory)
Cortex (somatosensory)
Electrophysiological Phenomena
Hippocampus - cytology
Hippocampus - physiology
Hypothalamus
Infants
Juveniles
Male
Mapping
Mice
Mice, Inbred C57BL
Neural Inhibition
Neural Pathways - physiology
Neurons
Neurons - physiology
Oxytocin
Parental behavior
Paternal Behavior
Preoptic area
Preoptic Area - cytology
Preoptic Area - physiology
Projection
Receptors
Receptors, Oxytocin - metabolism
Social Behavior
Social Environment
Stimuli
Thalamus
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Summary:Male animals may show alternative behaviors toward infants: attack or parenting. These behaviors are triggered by pup stimuli under the influence of the internal state, including the hormonal environment and/or social experiences. Converging data suggest that the medial preoptic area (MPOA) contributes to the behavioral selection toward the pup. However, the neural mechanisms underlying how integrated stimuli affect the MPOA-dependent behavioral selection remain unclear. Here we focus on the amygdalohippocampal area (AHi) that projects to MPOA and expresses oxytocin receptor, a hormone receptor mediating social behavior toward pups. We describe the activation of MPOA-projection AHi neurons in male mice by social contact with pups. Input mapping using the TRIO method reveals that MPOA-projection AHi neurons receive prominent inputs from several regions, including the thalamus, hypothalamus, and olfactory cortex. Electrophysiological and histologic analysis demonstrates that oxytocin modulates inhibitory synaptic responses on MPOA-projection AHi neurons. In addition, AHi forms the excitatory monosynapse to MPOA, and pharmacological activation of MPOA-projection AHi neurons enhances only aggressive behavior, but not parental behavior. Interestingly, this promoted behavior was related to social experience in male mice. Collectively, our results identified a presynaptic partner of MPOA that can integrate sensory input and hormonal state, and trigger pup-directed aggression. The medial preoptic area (MPOA) plays critical roles in parental behavior, such as motor control, motivation, and social interaction. The MPOA projects to multiple brain regions, and these projections contribute to several neural controls in parental behavior. In contrast, how inputs to MPOA are regulated by social and environmental information is poorly understood. In this study, we focus on the amygdalohippocampal area (AHi) that connects to MPOA and expresses oxytocin receptor. We demonstrate the disruption of the expression of parental behavior triggered by the activation of MPOA-projection AHi neurons. This behavior may be regulated not only by oxytocin but also by neural input from several regions.
ISSN:0270-6474
1529-2401
DOI:10.1523/JNEUROSCI.0438-19.2020