Intergenerational Sex-Specific Transmission of Maternal Social Experience
Jamshid Faraji, Mitra Karimi, Nabiollah Soltanpour, Zahra Rouhzadeh, Shabnam Roudaki, S Abedin Hosseini, S Yaghoob Jafari, Ali-Akbar Abdollahi, Nasrin Soltanpour, Reza Moeeini, Gerlinde A S Metz, Jamshid Faraji, Mitra Karimi, Nabiollah Soltanpour, Zahra Rouhzadeh, Shabnam Roudaki, S Abedin Hosseini, S Yaghoob Jafari, Ali-Akbar Abdollahi, Nasrin Soltanpour, Reza Moeeini, Gerlinde A S Metz
Abstract
The social environment is a major determinant of individual stress response and lifetime health. The present study shows that (1) social enrichment has a significant impact on neuroplasticity and behaviour particularly in females; and (2) social enrichment in females can be transmitted to their unexposed female descendants. Two generations (F0 and F1) of male and female rats raised in standard and social housing conditions were examined for neurohormonal and molecular alterations along with changes in four behavioural modalities. In addition to higher cortical neuronal density and cortical thickness, social experience in mothers reduced hypothalamic-pituitary-adrenal (HPA) axis activity in F0 rats and their F1 non-social housing offspring. Only F0 social mothers and their F1 non-social daughters displayed improved novelty-seeking exploratory behaviour and reduced anxiety-related behaviour whereas their motor and cognitive performance remained unchanged. Also, cortical and mRNA measurements in the F1 generation were affected by social experience intergenerationally via the female lineage (mother-to-daughter). These findings indicate that social experience promotes cortical neuroplasticity, neurohormonal and behavioural outcomes, and these changes can be transmitted to the F1 non-social offspring in a sexually dimorphic manner. Thus, a socially stimulating environment may form new biobehavioural phenotypes not only in exposed individuals, but also in their intergenerationally programmed descendants.
Conflict of interest statement
The authors declare no competing interests.
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References
- Rosenzweig MR, Bennett EL, Hebert M, Morimoto H. Social grouping cannot account for cerebral effects of enriched environments. Brain research. 1978;153:563–576. doi: 10.1016/0006-8993(78)90340-2.
- Krech D, Rosenzweig MR, Bennett EL. Effects of environmental complexity and training on brain chemistry. Journal of comparative and physiological psychology. 1960;53:509–519. doi: 10.1037/h0045402.
- Rosenzweig MR, Krech D, Bennett EL, Diamond MC. Effects of environmental complexity and training on brain chemistry and anatomy: a replication and extension. Journal of comparative and physiological psychology. 1962;55:429–437. doi: 10.1037/h0041137.
- McCreary JK, Erickson ZT, Metz GA. Environmental enrichment mitigates the impact of ancestral stress on motor skill and corticospinal tract plasticity. Neuroscience letters. 2016;632:181–186. doi: 10.1016/j.neulet.2016.08.059.
- Reynolds S, Lane SJ, Richards L. Using animal models of enriched environments to inform research on sensory integration intervention for the rehabilitation of neurodevelopmental disorders. Journal of neurodevelopmental disorders. 2010;2:120–132. doi: 10.1007/s11689-010-9053-4.
- Welberg L, Thrivikraman KV, Plotsky PM. Combined pre- and postnatal environmental enrichment programs the HPA axis differentially in male and female rats. Psychoneuroendocrinology. 2006;31:553–564. doi: 10.1016/j.psyneuen.2005.11.011.
- McCreary JK, et al. Environmental Intervention as a Therapy for Adverse Programming by Ancestral Stress. Scientific reports. 2016;6:37814. doi: 10.1038/srep37814.
- Welch BL, Brown DG, Welch AS, Lin DC. Isolation, restrictive confinement or crowding of rats for one year. I. Weight, nucleic acids and protein of brain regions. Brain research. 1974;75:71–84. doi: 10.1016/0006-8993(74)90771-9.
- Renner MJ, Rosenzweig MR. Social interactions among rats housed in grouped and enriched conditions. Dev Psychobiol. 1986;19:303–313. doi: 10.1002/dev.420190403.
- Faraji J, et al. Stress inhibits psychomotor performance differently in simple and complex open field environments. Hormones and behavior. 2014;65:66–75. doi: 10.1016/j.yhbeh.2013.11.007.
- Faraji J, et al. Stress enhances return-based behaviors in Wistar rats during spatial navigation without altering spatial performance: improvement or deficit? Physiology & behavior. 2013;122:163–171. doi: 10.1016/j.physbeh.2013.08.021.
- Wallace JE, Krauter EE, Campbell BA. Motor and reflexive behavior in the aging rat. J Gerontol. 1980;35:364–370. doi: 10.1093/geronj/35.3.364.
- Pellow S, Chopin P, File SE, Briley M. Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods. 1985;14:149–167. doi: 10.1016/0165-0270(85)90031-7.
- Faraji J, Gomez-Palacio-Schjetnan A, Luczak A, Metz GA. Beyond the silence: bilateral somatosensory stimulation enhances skilled movement quality and neural density in intact behaving rats. Behavioural brain research. 2013;253:78–89. doi: 10.1016/j.bbr.2013.07.022.
- Hall CS. Emotional behaviour in the rat. I. Defecation and urination asmeasures of individual differences in emotionality. J. Comp. Psychol. 1934;18:385–403. doi: 10.1037/h0071444.
- Nemati F, Kolb B, Metz GA. Stress and risk avoidance by exploring rats: implications for stress management in fear-related behaviours. Behav Processes. 2013;94:89–98. doi: 10.1016/j.beproc.2012.12.005.
- Ambeskovic, M. et al. Ancestral Exposure to Stress Generates New Behavioral Traits and a Functional Hemispheric Dominance Shift. Cerebral cortex (New York, N.Y.: 1991), 10.1093/cercor/bhw063 (2016).
- Jacobsen JP, Mork A. The effect of escitalopram, desipramine, electroconvulsive seizures and lithium on brain-derived neurotrophic factor mRNA and protein expression in the rat brain and the correlation to 5-HT and 5-HIAA levels. Brain Res. 2004;1024:183–192. doi: 10.1016/j.brainres.2004.07.065.
- Ward ID, et al. Transgenerational programming of maternal behaviour by prenatal stress. BMC pregnancy and childbirth. 2013;13(Suppl 1):S9. doi: 10.1186/1471-2393-13-S1-S9.
- Meaney MJ, Szyf M, Seckl JR. Epigenetic mechanisms of perinatal programming of hypothalamic-pituitary-adrenal function and health. Trends in molecular medicine. 2007;13:269–277. doi: 10.1016/j.molmed.2007.05.003.
- Champagne FA. Epigenetic mechanisms and the transgenerational effects of maternal care. Frontiers in neuroendocrinology. 2008;29:386–397. doi: 10.1016/j.yfrne.2008.03.003.
- Morgan CP, Bale TL. Early prenatal stress epigenetically programs dysmasculinization in second-generation offspring via the paternal lineage. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2011;31:11748–11755. doi: 10.1523/JNEUROSCI.1887-11.2011.
- Kolb B, Stewart J. Sex-related differences in dendritic branching of cells in the prefrontal cortex of rats. Journal of neuroendocrinology. 1991;3:95–99. doi: 10.1111/j.1365-2826.1991.tb00245.x.
- Pilgrim C, Hutchison JB. Developmental regulation of sex differences in the brain: can the role of gonadal steroids be redefined? Neuroscience. 1994;60:843–855. doi: 10.1016/0306-4522(94)90267-4.
- Swain JE, et al. Approaching the biology of human parental attachment: brain imaging, oxytocin and coordinated assessments of mothers and fathers. Brain research. 2014;1580:78–101. doi: 10.1016/j.brainres.2014.03.007.
- Hillerer KM, Jacobs VR, Fischer T, Aigner L. The maternal brain: an organ with peripartal plasticity. Neural plasticity. 2014;2014:574159. doi: 10.1155/2014/574159.
- Ayers LW, Missig G, Schulkin J, Rosen JB. Oxytocin reduces background anxiety in a fear-potentiated startle paradigm: peripheral vs central administration. Neuropsychopharmacology: official publication of the American College of Neuropsychopharmacology. 2011;36:2488–2497. doi: 10.1038/npp.2011.138.
- Kolb B, Gibb R. Plasticity in the prefrontal cortex of adult rats. Frontiers in cellular neuroscience. 2015;9:15. doi: 10.3389/fncel.2015.00015.
- Burke AR, McCormick CM, Pellis SM, Lukkes JL. Impact of adolescent social experiences on behavior and neural circuits implicated in mental illnesses. Neuroscience and biobehavioral reviews. 2017;76:280–300. doi: 10.1016/j.neubiorev.2017.01.018.
- Kolb B. Social behavior of rats with chronic prefrontal lesions. Journal of comparative and physiological psychology. 1974;87:466–474. doi: 10.1037/h0036969.
- Bell HC, Pellis SM, Kolb B. Juvenile peer play experience and the development of the orbitofrontal and medial prefrontal cortices. Behavioural brain research. 2010;207:7–13. doi: 10.1016/j.bbr.2009.09.029.
- van Kerkhof LW, Damsteegt R, Trezza V, Voorn P, Vanderschuren LJ. Social play behavior in adolescent rats is mediated by functional activity in medial prefrontal cortex and striatum. Neuropsychopharmacology: official publication of the American College of Neuropsychopharmacology. 2013;38:1899–1909. doi: 10.1038/npp.2013.83.
- de Kloet ER, Oitzl MS, Joels M. Stress and cognition: are corticosteroids good or bad guys? Trends in neurosciences. 1999;22:422–426. doi: 10.1016/S0166-2236(99)01438-1.
- Meaney MJ, et al. Cellular mechanisms underlying the development and expression of individual differences in the hypothalamic-pituitary-adrenal stress response. The Journal of steroid biochemistry and molecular biology. 1991;39:265–274. doi: 10.1016/0960-0760(91)90072-D.
- Metz GA, Ng JW, Kovalchuk I, Olson DM. Ancestral experience as a game changer in stress vulnerability and disease outcomes. BioEssays: news and reviews in molecular, cellular and developmental biology. 2015;37:602–611. doi: 10.1002/bies.201400217.
- Cottrell EC, Seckl JR. Prenatal stress, glucocorticoids and the programming of adult disease. Frontiers in behavioral neuroscience. 2009;3:19. doi: 10.3389/neuro.08.019.2009.
- Yao Y, et al. Ancestral exposure to stress epigenetically programs preterm birth risk and adverse maternal and newborn outcomes. BMC Med. 2014;12:121. doi: 10.1186/s12916-014-0121-6.
- Welberg LA, Thrivikraman KV, Plotsky PM. Chronic maternal stress inhibits the capacity to up-regulate placental 11beta-hydroxysteroid dehydrogenase type 2 activity. The Journal of endocrinology. 2005;186:R7–r12. doi: 10.1677/joe.1.06374.
- Noorlander CW, De Graan PN, Middeldorp J, Van Beers JJ, Visser GH. Ontogeny of hippocampal corticosteroid receptors: effects of antenatal glucocorticoids in human and mouse. The Journal of comparative neurology. 2006;499:924–932. doi: 10.1002/cne.21162.
- DeVries AC, Glasper ER, Detillion CE. Social modulation of stress responses. Physiology & behavior. 2003;79:399–407. doi: 10.1016/S0031-9384(03)00152-5.
- Stead JD, et al. Selective breeding for divergence in novelty-seeking traits: heritability and enrichment in spontaneous anxiety-related behaviors. Behavior genetics. 2006;36:697–712. doi: 10.1007/s10519-006-9058-7.
- Stack A, et al. Sex differences in social interaction in rats: role of the immediate-early gene zif268. Neuropsychopharmacology: official publication of the American College of Neuropsychopharmacology. 2010;35:570–580. doi: 10.1038/npp.2009.163.
- Nofrey B, Rocha B, Lopez HH, Ettenberg A. The effects of sexual experience and estrus on male-seeking motivated behavior in the female rat. Physiology & behavior. 2008;95:533–538. doi: 10.1016/j.physbeh.2008.08.002.
- Rossi C, et al. Brain-derived neurotrophic factor (BDNF) is required for the enhancement of hippocampal neurogenesis following environmental enrichment. The European journal of neuroscience. 2006;24:1850–1856. doi: 10.1111/j.1460-9568.2006.05059.x.
- Bustamante C, et al. Maternal exercise during pregnancy ameliorates the postnatal neuronal impairments induced by prenatal restraint stress in mice. International journal of developmental neuroscience: the official journal of the International Society for Developmental Neuroscience. 2013;31:267–273. doi: 10.1016/j.ijdevneu.2013.02.007.
- Blaze J, Asok A, Roth TL. Long-term effects of early-life caregiving experiences on brain-derived neurotrophic factor histone acetylation in the adult rat mPFC. Stress (Amsterdam, Netherlands) 2015;18:607–615. doi: 10.3109/10253890.2015.1071790.
- Ghassabian, A. et al. Determinants of neonatal brain-derived neurotrophic factor and association with child development. Development and psychopathology, 1–13, 10.1017/s0954579417000414 (2017).
- Mashoodh R, Franks B, Curley JP, Champagne FA. Paternal social enrichment effects on maternal behavior and offspring growth. Proceedings of the National Academy of Sciences of the United States of America. 2012;109(Suppl 2):17232–17238. doi: 10.1073/pnas.1121083109.
- Gapp K, von Ziegler L, Tweedie-Cullen RY, Mansuy IM. Early life epigenetic programming and transmission of stress-induced traits in mammals: how and when can environmental factors influence traits and their transgenerational inheritance? BioEssays: news and reviews in molecular, cellular and developmental biology. 2014;36:491–502. doi: 10.1002/bies.201300116.
- Hennessy MB, Heybach JP, Vernikos J, Levine S. Plasma corticosterone concentrations sensitively reflect levels of stimulus intensity in the rat. Physiology & behavior. 1979;22:821–825. doi: 10.1016/0031-9384(79)90321-4.
- Kazlauckas V, et al. Behavioral and cognitive profile of mice with high and low exploratory phenotypes. Behavioural brain research. 2005;162:272–278. doi: 10.1016/j.bbr.2005.03.021.
- Babenko O, Kovalchuk I, Metz GA. Stress-induced perinatal and transgenerational epigenetic programming of brain development and mental health. Neuroscience and biobehavioral reviews. 2015;48:70–91. doi: 10.1016/j.neubiorev.2014.11.013.
- Gapp K, et al. Early life stress in fathers improves behavioural flexibility in their offspring. Nature communications. 2014;5:5466. doi: 10.1038/ncomms6466.
- Uller T. Developmental plasticity and the evolution of parental effects. Trends Ecol Evol. 2008;23:432–438. doi: 10.1016/j.tree.2008.04.005.
- Curley JP, Mashoodh R, Champagne FA. Epigenetics and the origins of paternal effects. Hormones and behavior. 2011;59:306–314. doi: 10.1016/j.yhbeh.2010.06.018.
- Mychasiuk R, Metz GA. Epigenetic and gene expression changes in the adolescent brain: What have we learned from animal models? Neuroscience and biobehavioral reviews. 2016;70:189–197. doi: 10.1016/j.neubiorev.2016.07.013.
- Nithianantharajah J, Hannan AJ. Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nature reviews. Neuroscience. 2006;7:697–709. doi: 10.1038/nrn1970.
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