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Projection Sites of Medial Preoptic Area and Ventral Bed Nucleus of the Stria Terminalis Neurons that Express Fos during Maternal Behavior in Female Rats
Abstract
Medial preoptic area (MPOA) and ventral bed nucleus of the stria terminalis (VBST) neurons are involved in maternal behavior, but the neural sites to which the maternally relevant neurons project have not been determined. Since MPOA and VBST neurons express Fos during maternal behavior, we used a double‐labeling immunocytochemical procedure to detect both Fos and a retrograde tracer, wheat germ agglutinin (WGA), in order to determine where these Fos neurons project. On Day 4 postpartum, fully maternal females were separated from their litters. On Day 5, WGA was iontophoretically injected into one of the following regions known to receive MPOA and/or VBST input: Lateral septum, medial hypothalamus at the level of the ventromedial nucleus, lateral habenula, ventral tegmental area, retrorubral field, or periaqueductal gray. On Day 7, females received a 2‐h test with either pups or candy, after which they were perfused and their brains were processed for the detection of Fos and WGA. As expected, females tested with pups had more Fos‐containing neurons in the MPOA and VBST than did females tested with candy. After WGA injections into several brain sites, the number of double‐labeled cells observed in the MPOA and VBST was greater for the maternal females when compared to the non‐maternal females. Therefore, these results pinpointed neural circuits that were activated during maternal behavior. For the maternal females, Fos‐containing neurons in the MPOA projected most strongly to the medial hypothalamus at the level of the ventromedial nucleus and to the lateral septum, while Fos‐containing neurons in the VBST projected most strongly to the retrorubral field, ventral tegmental area, and medial hypothalamus. Although relatively few MPOA and VBST neurons which expressed Fos during maternal behavior projected to the periaqueductal gray, these Fos‐expressing neurons made up a relatively large proportion of the MPOA and VBST projection to the periaqueductal gray. This study suggests that MPOA and VBST efferents project to a variety of regions to promote full maternal responsiveness.
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Oxytocin activates c-Fos positive neurons.
“which are now known to activate c-Fos positive neurons51–53.”
From Vascular RAGE transports oxytocin into the brain to elicit its maternal bonding behaviour in mice (2019) · cites this paper as [51]
c-Fos positive neurons are activated during the acquisition of postpartum maternal behaviours.
“The classical studies of Numan showed c-Fos positive neurons are activated during the acquisition of postpartum maternal behaviours51.”
From Vascular RAGE transports oxytocin into the brain to elicit its maternal bonding behaviour in mice (2019) · cites this paper as [51]
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“In addition, MPOA cells activated during maternal care project to the anterior hypothalamic nucleus, ventral tegmental area, periaqueductal gray, and retrorubral field [17].”
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“The vBNST has been implicated in maternal behavior (Numan & Numan, 1997), cocaine CPP expression (Sartor & Aston-Jones, 2012), and heroin-primed reinstatement (Rogers et al., 2008), whereas the medial posterior (mpBNST) subdivision is involved in both heroin- and cueprimed reinstatement (Rogers et…”
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“The iontophoretic administration of anterograde (Phaseolus vulgaris Leucoaglutinin; Numan & Numan, 1996) and retrograde (wheat germ agglutinin: WGA; Numan & Numan, 1997) tracers in the rat, revealed projections from MPOA and their adjacent ventral bed nucleus of the stria terminalis, vBNST, to important areas related…”
BackgroundSmith, C. D., Holschbach, M., Olsewicz, J., & Lonstein, J. S. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2749-2 · Cited by 29
“The BSTv and mPOA are activated by offspring sensory cues (Fleming et al. 1994; Kalinichev et al. 2000; Lonstein et al. 1998) and can influence behavioral inhibition or activation via projections to sites involved in locomotion (Numan and Numan 1997).”
InfluentialToward a systems-oriented approach to the role of the extended amygdala in adaptive responding
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“Because it was established that some brain regions receiving projections from MPOA neurons are part of the defensive circuits and inhibit maternal care (Numan and Numan, 1997), in the present paper, we also addressed if projections of inhibitory neurons to these brain regions are sexually dimorphic.”
BackgroundMaternal care activates the ventral tegmental area but not dopaminergic cells in the rat
Caba, M., Melo, Á. I., Fleming, A. S., & Meza, E. (2019) · Journal of Neuroendocrinology · doi:10.1111/jne.12713 · Cited by 25
Mann, P. E., & Babb, J. A. (2004) · Brain Research · doi:10.1016/j.brainres.2004.07.064 · Cited by 22
Molecular neuroanatomy of the mouse medial preoptic area with reference to parental behavior
Tsuneoka, Y. (2018) · Anatomical Science International · doi:10.1007/s12565-018-0468-4 · Cited by 22
Neuroendocrinology and Neurochemistry of Maternal Motivation and Behavior
Lonstein, J. S., & Morrell, J. I. (2006) · Springer eBooks · doi:10.1007/978-0-387-30405-2_5 · Cited by 23
Numan, M., & Stolzenberg, D. S. (2008) · Elsevier eBooks · doi:10.1016/b978-0-12-374285-8.00001-9 · Cited by 22
Self-citationWaraczynski, M. A., & Perkins, M. G. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02908-5 · Cited by 21
Maternal care associates with differences in morphological complexity in the medial preoptic area
Parent, C. I., Wen, X., Dhir, S. K., Ryan, R., Diorio, J. C., & Zhang, T. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.02.047 · Cited by 20
“Paradis, A loss-of-function analysis reveals that endogenous Rem2 promotes functional glutamatergic synapse formation and restricts dendritic complexity, PLoS One 8 (8) (2013) e74751.”
Cannabinoid receptor agonist disrupts behavioral and neuroendocrine responses during lactation
Vilela, F. C., & Giusti‐Paiva, A. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.01.037 · Cited by 20
Kelm‐Nelson, C. A., & Riters, L. V. (2013) · Brain Research · doi:10.1016/j.brainres.2013.06.010 · Cited by 19
“…al., 2011; Mansour et al., 1994; Pilapil et al., 1987; Riters et al., 2005; Sar et al., 1978; Woods et al., 2010) neural circuit that has been implicated in affiliative social behavior (e.g., (Lonstein and De Vries, 2000; Numan and Numan, 1997)) in birds and mammals (Goodson, 2005; Newman, 1999).”
BackgroundNi, R., Luo, P.-H., Shu, Y., Chen, J., & Zhou, J. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.07.017 · Cited by 19
Central Nitric Oxide Synthase Inhibition Disrupts Maternal Behavior in the Rat.
Popeski, N., & Woodside, B. C. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.6.1305 · Cited by 18
Social behavior in prepubertal neurexin 1α deficient rats: A model of neurodevelopmental disorders.
Kight, K. E., Argue, K. J., Bumgardner, J. G., Bardhi, K., Waddell, J., & McCarthy, M. M. (2021) · Behavioral Neuroscience · doi:10.1037/bne0000482 · Cited by 17
The developmental mechanisms and the signal functions of early infant crying
Soltis, J. M. (2004) · Behavioral and Brain Sciences · doi:10.1017/s0140525x0442010x · Cited by 15
Detection of neural connections with ex vivo MRI using a ferritin-encoding trans-synaptic virus
Zheng, N., Su, P., Liu, Y., Wang, H., Nie, B., Fang, X., Xu, Y., Lin, K., Lv, P., He, X., et al. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.04.039 · Cited by 15
“, 1993), wheat germ 51 agglutinin (Numan and Numan, 1997), tetanus cholera B fragment (Lai et al.”
BackgroundSinpru, P., Porter, T. E., Halawani, M. E. E., & Chaiseha, Y. (2017) · Acta Histochemica · doi:10.1016/j.acthis.2017.09.002 · Cited by 12
Hewlett, S. E., Zeinstra, E. C., Eerdenburg, F. J. C. M. V., Rodenburg, T. B., van Kooten, P. J. S., van der Staay, F. J., & Nordquist, R. E. (2014) · BMC Veterinary Research · doi:10.1186/1746-6148-10-167 · Cited by 12
“The MPA is heavily involved in expression of maternal behavior, and the presence of pups increases the activity of the MPA in female rats [45].”
BackgroundEarly infant crying as a behavioral state rather than a signal
Barr, R. G. (2004) · Behavioral and Brain Sciences · doi:10.1017/s0140525x04230102 · Cited by 12
Dudas, A., Nakahara, T. S., Pellissier, L. P., & Chamero, P. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105686 · Cited by 11
“(Kohl et al., 2018, 2017; Kohl and Dulac, 2018; Numan and Numan, 1997; Tsuneoka et al., 2015, 2013; Wu et al., 2014).”
Metadata
- Authors
- Numan, M., & Numan, M. J.
- Affiliations
- Boston College (US)
- Corresponding author
- Numan, Michael
- Venue
- Journal of Neuroendocrinology
- Publisher
- Wiley
- Published
- 1997-05
- Volume
- 9
- Issue
- 5
- Pages
- 369-384
- ISSN
- 0953-8194 (ISSN-L)
- 1365-2826
- OpenAlex
- W2116801697
- Cited by
- 149
- References
- 0
- Citations by year
- 2025: 2 · 2024: 5 · 2023: 1 · 2022: 3 · 2021: 7 · 2020: 16 · 2019: 11 · 2018: 6 · 2017: 6 · 2016: 5 · 2015: 5 · 2014: 8 · 2013: 5 · 2012: 3
- FWCI
- 12.05
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neuroendocrinology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Keywords
- maternal behavior, medial preoptic area, Fos expression, retrograde tracing, wheat germ agglutinin, lateral septum, ventromedial hypothalamus, periaqueductal gray, ventral tegmental area, retrorubral field, lateral habenula
- MeSH terms
- Animals, Female, Hypothalamus, Immunohistochemistry, Maternal Behavior, Nerve Tissue Proteins, Neural Pathways, Neurons, Preoptic Area, Wheat Germ Agglutinins, Proto-Oncogene Proteins c-fos, Rats
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