Behavioral transition from attack to parenting in male mice: a crucial role of the vomeronasal system
Open accessAbstract
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.
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Responses of VNO sensory neurons can be modulated by hormones, internal status, and sensory experience in a sex-specific manner.
“Indeed, a number of studies have shown that responses of VNO sensory neurons can be modulated by hormones, internal status, and sensory experience in a sex-specific manner (Dey et al., 2015; Halem et al., 2001; Tachikawa et al., 2013; Xu et al., 2016).”
From Neuronal Representation of Social Information in the Medial Amygdala of Awake Behaving Mice (2017) · cites this paper as Tachikawa et al., 2013
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- Authors
- Tachikawa, K. S., Yoshihara, Y., & Kuroda, K. O.
- Affiliations
- RIKEN Center for Brain Science (JP)
- RIKEN (JP)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2013-03-20
- Volume
- 33
- Issue
- 12
- Pages
- 5120-5126
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6705007
- OpenAlex
- W2029922574
- Cited by
- 192
- References
- 28
- Citations by year
- 2026: 11 · 2025: 21 · 2024: 15 · 2023: 10 · 2022: 17 · 2021: 18 · 2020: 30 · 2019: 13 · 2018: 14 · 2017: 6 · 2016: 13 · 2015: 10 · 2014: 12 · 2013: 2
- FWCI
- 18.46
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Tokyo Tech Research Repository (Tokyo Institute of Technology) (submittedVersion)
- Funders
- Japan Society for the Promotion of Science (23700420)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- paternal behavior, vomeronasal system, vomeronasal sensory neurons, chemical cues, behavioral transitions, accessory olfactory bulb, bed nucleus of the stria terminalis, anterior hypothalamic area, c-Fos neuronal activation, male mice, fatherhood
- MeSH terms
- Aggression, Amygdala, Animals, Behavior, Animal, Copulation, Female, Anterior Hypothalamic Nucleus, Male, Mice, Inbred C57BL, Olfactory Bulb, Paternal Behavior, Pheromones, Pregnancy, Proto-Oncogene Proteins c-fos, Vomeronasal Organ, Mice
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