Neurogenesis and anxiety-like behavior in male California mice during the mate’s postpartum period
Abstract
Our understanding of postpartum anxiety (PPA) in fathers is limited, despite the negative consequences of anxiety on the father and child. Offspring contact reduces PPA in mothers; however, parallel investigations in fathers has gone unaddressed. Adult neurogenesis in the dentate gyrus (DG) contributes to anxiety regulation and is altered during the postpartum period, yet the effects of fatherhood on the production, or survival, of newborn cells in the DG, and the role of adult neurogenesis in PPA regulation, have not been examined. Using the biparental California mouse (Peromyscus californicus), we examined the relationships among postnatal day, anxiety-like behavior and adult neurogenesis in fathers. We hypothesized that attenuated anxiety-like behavior and enhanced adult neurogenesis would be observed when father-offspring contact was increased. We observed a reduction in anxiety-like behavior on the elevated plus-maze, but only at PND 16, a time of peak pup retrieval. Fatherhood reduced 1-week survival of newborn cells; however, surviving cells were maintained until 2 weeks postpartum. In contrast, non-fathers experienced a significant reduction in the survival of newborn cells between 1 and 2 weeks postpartum. Fatherhood also increased the numbers of newborn cells that expressed a neuronal phenotype. Collectively, these findings suggest that offspring interaction contributes to reductions in anxiety-like behavior and the maintenance of newborn neurons in the DG of fathers. These data contribute to our knowledge of the postpartum affective state in fathers, findings that may contribute to improved health of both the father and offspring.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Parenting has suppressive effects on adult neurogenesis in both mothers and fathers.
“In both mothers and fathers, parenting has suppressive effects on adult neurogenesis (Darnaudéry et al., 2007; Glasper et al., 2011; Hyer et al., 2016; Leuner et al., 2007; Pawluski and Galea, 2007; Mahmoud et al., 2016).”
From Adult neurogenesis, glia, and the extracellular matrix (2019) · cites this paper as Hyer et al., 2016
Cites
The mouse brain in stereotaxic coordinates
Konsman, J. (2003) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(03)00088-x · Cited by 16,796 · see citing works
The use of the elevated plus maze as an assay of anxiety-related behavior in rodents
Walf, A. A., & Frye, C. A. (2007) · Nature Protocols · doi:10.1038/nprot.2007.44 · Cited by 3,035 · see citing works
West, M. J., Slomianka, L., & Gundersen, H. J. G. (1991) · The Anatomical Record · doi:10.1002/ar.1092310411 · Cited by 2,994 · cited 2× · see citing works
“…(granule layer, subgranular zone and hilus) and basolateral amygdala were counted at 100 9 magnification under oil immersion on a Zeiss Primo Star light microscope (Zeiss, Thornwood, NY, USA) by using a modified version of the optical fractionator method (West et al., 1991; Ngwenya et al., 2005).”
MethodAmygdala circuitry mediating reversible and bidirectional control of anxiety
Tye, K. M., Prakash, R., Kim, S.-Y., Fenno, L. E., Grosenick, L., Zarabi, H., Thompson, K. R., Gradinaru, V., Ramakrishnan, C., & Deisseroth, K. (2011) · Nature · doi:10.1038/nature09820 · Cited by 1,289 · see citing works
Differential Control of Learning and Anxiety along the Dorsoventral Axis of the Dentate Gyrus
Kheirbek, M. A., Drew, L. J., Burghardt, N. S., Costantini, D. O., Tannenholz, L., Ahmari, S. E., Zeng, H., Fenton, A. A., & Hen, R. (2013) · Neuron · doi:10.1016/j.neuron.2012.12.038 · Cited by 713 · see citing works
How widespread is adult neurogenesis in mammals?
Gould, E. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2147 · Cited by 658 · see citing works
Adult hippocampal neurogenesis is involved in anxiety-related behaviors
Revest, J.-M., Dupret, D., Koehl, M., Funk-Reiter, C., Grosjean, N., Piazza, P.-V., & Abrous, D. N. (2009) · Molecular Psychiatry · doi:10.1038/mp.2009.15 · Cited by 549 · see citing works
Combinatorial roles of the nuclear receptor corepressor in transcription and development.
Jepsen, K., Hermanson, O., Onami, T. M., Gleiberman, A., Lunyak, V., Mcevilly, R., Kurokawa, R., Kumar, V., Liu, F. C., Seto, E., et al. (2000) · Cell · doi:10.1016/s0092-8674(00)00064-7 · Cited by 545 · see citing works
Structural Plasticity and Hippocampal Function
Leuner, B., & Gould, E. (2009) · Annual Review of Psychology · doi:10.1146/annurev.psych.093008.100359 · Cited by 452 · see citing works
Barrett, J., & Fleming, A. S. (2011) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2010.02306.x · Cited by 433 · see citing works
Testosterone and prolactin are associated with emotional responses to infant cries in new fathers
Fleming, A. S., Corter, C., Stallings, J., & Steiner, M. (2002) · Hormones and Behavior · doi:10.1006/hbeh.2002.1840 · Cited by 401 · see citing works
Paternal psychiatric disorders and children's psychosocial development
Ramchandani, P., & Psychogiou, L. (2009) · The Lancet · doi:10.1016/s0140-6736(09)60238-5 · Cited by 359 · see citing works
Long-term behavioural and molecular alterations associated with maternal separation in rats
Lippmann, M., Bress, A., Nemeroff, C. B., Plotsky, P. M., & Monteggia, L. M. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05522.x · Cited by 355 · see citing works
A systematic review of the effects of postnatal maternal anxiety on children
Glasheen, C., Richardson, G. A., & Fabio, A. (2009) · Archives of Women s Mental Health · doi:10.1007/s00737-009-0109-y · Cited by 322 · see citing works
Bester‐Meredith, J. K., Young, L. J., & Marler, C. A. (1999) · Hormones and Behavior · doi:10.1006/hbeh.1999.1522 · Cited by 285 · see citing works
The biparental care system of the California mouse, Peromyscus californicus.
Gubernick, D. J., & Alberts, J. R. (1987) · Journal of comparative psychology · doi:10.1037/0735-7036.101.2.169 · Cited by 274 · see citing works
Torner, L., Toschi, N., Pohlinger, A., Landgraf, R., & Neumann, I. D. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-09-03207.2001 · Cited by 266 · see citing works
Hormonal Changes in Males of a Naturally Biparental and a Uniparental Mammal
Wheaton, C. J., & Wynne‐Edwards, K. E. (1999) · Hormones and Behavior · doi:10.1006/hbeh.1998.1509 · Cited by 245 · see citing works
Impact of Antenatal and Postpartum Maternal Mental Illness: How are the Children?
Brand, S. R., & Brennan, P. A. (2009) · Clinical Obstetrics & Gynecology · doi:10.1097/grf.0b013e3181b52930 · Cited by 231 · see citing works
Regulation of anxiety during the postpartum period
Lonstein, J. S. (2007) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2007.05.002 · Cited by 229 · see citing works
Reproductive experience alters hippocampal neurogenesis during the postpartum period in the dam
Pawluski, J. L., & Galea, L. A. M. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.07.031 · Cited by 209 · see citing works
Paternal recognition of adult offspring mediated by newly generated CNS neurons
Mak, G. K., & Weiss, S. (2010) · Nature Neuroscience · doi:10.1038/nn.2550 · Cited by 201 · see citing works
Prolactin and parental behaviour in a male New World primate
Dixson, A. F., & George, L. (1982) · Nature · doi:10.1038/299551a0 · Cited by 186 · see citing works
Leuner, B., Mirescu, C., Noiman, L., & Gould, E. (2007) · Hippocampus · doi:10.1002/hipo.20278 · Cited by 174 · see citing works
Macbeth, A. H., & Luine, V. N. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.08.011 · Cited by 169 · see citing works
Prolactin and paternal behavior in the biparental California mouse, Peromyscus californicus
Gubernick, D. J., & Nelson, R. J. (1989) · Hormones and Behavior · doi:10.1016/0018-506x(89)90061-5 · Cited by 167 · see citing works
Leuner, B., Glasper, E. R., & Gould, E. (2010) · Trends in Neurosciences · doi:10.1016/j.tins.2010.07.003 · Cited by 159 · see citing works
Lonstein, J. S. (2005) · Hormones and Behavior · doi:10.1016/j.yhbeh.2004.11.001 · Cited by 147 · see citing works
Primate paternal care: Interactions between biology and social experience
Storey, A. E., & Ziegler, T. E. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.07.024 · Cited by 111 · see citing works
Maniam, J., & Morris, M. J. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.11.005 · Cited by 104 · see citing works
Sung, Y.-H., Shin, M.-S., Cho, S., Baik, H., Jin, B., Chang, H.-K., Lee, E.-K., & Kim, C.-J. (2010) · Neuroscience Letters · doi:10.1016/j.neulet.2009.12.063 · Cited by 87 · see citing works
Thymidine analog methods for studies of adult neurogenesis are not equally sensitive
Leuner, B., Glasper, E. R., & Gould, E. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22107 · Cited by 84 · see citing works
Self-citationZiegler, T. E., Prudom, S. L., Zahed, S. R., Parlow, A. F., & Wegner, F. H. (2009) · Hormones and Behavior · doi:10.1016/j.yhbeh.2009.07.012 · Cited by 73 · see citing works
Glasper, E. R., Kozorovitskiy, Y., Pavlic, A., & Gould, E. (2011) · Journal of Comparative Neurology · doi:10.1002/cne.22628 · Cited by 66 · cited 5× · see citing works
“E-mail: eglasper@umd.edu © 2016 Federation of European Neuroscience Societies and John Wiley & Sons Ltd females (Leuner et al., 2007; Pawluski & Galea, 2007; Glasper et al., 2011; Lieberwirth et al., 2013).”
BackgroundInfluentialAffective changes during the postpartum period: Influences of genetic and experiential factors
Agrati, D., & Lonstein, J. S. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.07.016 · Cited by 65 · see citing works
Roberts, R. L., Jenkins, K. T., Lawler, T., Wegner, F. H., & Newman, J. D. (2001) · Hormones and Behavior · doi:10.1006/hbeh.2000.1639 · Cited by 57 · see citing works
Ngwenya, L. B., Peters, A., & Rosene, D. L. (2005) · Journal of Histochemistry & Cytochemistry · doi:10.1369/jhc.4a6605.2005 · Cited by 53 · see citing works
Lieberwirth, C., Wang, Y., Jia, X., Liu, Y., & Wang, Z. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12323 · Cited by 48 · see citing works
Bredy, T. W., Brown, R. E., & Meaney, M. J. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05266.x · Cited by 44 · see citing works
Miyetani Chauke, A., A, T. R. D. J., Garland, T., & Wendy Saltzman, A. (2012) · Physiology & Behavior · doi:10.1016/j.physbeh.2012.05.012 · Cited by 41 · see citing works
Harris, B. N., Wendy Saltzman, A., A, T. R. D. J., & Milnes, M. R. (2012) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2012.08.026 · Cited by 40 · see citing works
Glasper, E. R., Hyer, M. M., Katakam, J., Harper, R., Ameri, C., & Wolz, T. (2015) · Brain and Behavior · doi:10.1002/brb3.416 · Cited by 33 · see citing works
Self-citationSocial and hormonal bases of individual differences in the parental behaviour of birds and mammals.
Storey, A. E., Delahunty, K. M., McKay, D. W., Walsh, C. J., & Wilhelm, S. I. (2006) · Canadian Journal of Experimental Psychology/Revue canadienne de psychologie expérimentale · doi:10.1037/cjep2006022 · Cited by 31 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Adult neurogenesis, glia, and the extracellular matrix
Cope, E. C., & Gould, E. (2019) · Cell Stem Cell · doi:10.1016/j.stem.2019.03.023 · Cited by 236 · see citing works
- Authors
- Hyer, M. M., Hunter, T. J., Katakam, J., Wolz, T., & Glasper, E. R.
- Affiliations
- University of Maryland, College Park (US)
- Corresponding author
- Glasper, E. R.
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 2016-02-15
- Volume
- 43
- Issue
- 5
- Pages
- 703-709
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- OpenAlex
- W2231804601
- Cited by
- 32
- References
- 43
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 2 · 2023: 2 · 2022: 1 · 2021: 2 · 2020: 2 · 2019: 6 · 2018: 10 · 2017: 2 · 2016: 1
- FWCI
- 3.23
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- European Journal of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- University of Maryland
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Keywords
- postpartum anxiety, paternal behavior, adult neurogenesis, dentate gyrus, newborn neuron survival, biparental care, Peromyscus californicus, anxiety-like behavior, elevated plus maze, postnatal development
- MeSH terms
- Animals, Anxiety, Fathers, Female, Male, Pregnancy, Pregnancy, Animal, Sexual Behavior, Animal, Dentate Gyrus, Mice, Neurogenesis
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
