Prenatal stress modifies hippocampal synaptic plasticity and spatial learning in young rat offspring

Abstract

Clinical studies demonstrate that prenatal stress causes cognitive deficits and increases vulnerability to affective disorders in children and adolescents. The underlying mechanisms are not yet fully understood. Here, we reported that prenatal stress (10 unpredictable, 1 s, 0.8 mA foot shocks per day during gestational days 13-19) impaired long-term potentiation (LTP) but facilitated long-term depression (LTD) in hippocampal CA1 region in slices of the prenatal stressed offspring (5 weeks old). Cross-fostering neonate offspring by the prenatal stressed or control mothers did not change the effects of prenatal stress on the hippocampal LTP and LTD. Furthermore, prenatal stress enhanced the effects of acute stress on the hippocampal LTP and LTD and impaired spatial learning and memory in the Morris water maze in the young rat offspring. Therefore, prenatal stress alters synaptic plasticity and enhances the effects of acute stress on synaptic plasticity in the hippocampus, which may be the mechanism for the impaired spatial learning and memory in young rat offspring.

Unraveling the Time Domains of Corticosteroid Hormone Influences on Brain Activity: Rapid, Slow, and Chronic Modes

“…More severe conditions, though, are consistently linked with reduced synaptic plasticity. This is true for prenatal stress (Kamphuis et al, 2003;Son et al, 2006;Yang et al, 2006Yang et al, , 2007Lee et al, 2011a;Yeh et al, 2012;but see Noorlander et al, 2008), low and/or fragmented maternal care including situations associated with impoverished environmental conditions (Bredy et al, 2003;Brunson et al, 2005;Cui et al, 2006;Champagne et al, 2008;Bagot et al, 2009Bagot et al, , 2012Ivy et al, 2010), prolonged maternal separation (Gruss et al, 2008;Stevenson et al, 2008;Oomen et al, 2010), or traumatic events (Akers et al, 2006;Judo et al, 2010). When investigated, basal synaptic properties or paired pulse responsiveness were not much altered (Domenici et al, 1996;Kamphuis et al, 2003;Yaka et al, 2007;Lee et al, 2011).…”

“…7), although interaction with other stress hormones is necessary to accomplish the full effect. The rapid depotentiation of LTP and shift toward LTD reported when animals are exposed to a (stressful) novel environment possibly plays a role in this phenomenon (Xu et al, 1997;ManahanVaughan and Braunewell, 1999;Yang et al, 2006;Hirata et al, 2009), although there is evidence that this is GR-rather than MR-dependent (Xu et al, 1998).…”

“…Enhanced LTP was reported for selective MR activation (Pavlides et al, 1996), particularly in the ventral-most part of the CA1 hippocampal area Segal, 2007, 2009b). GR activation not only impairs LTP induction but also slowly promotes LTD (Xiong et al, 2004;Yang et al, 2004Yang et al, , 2006Kim et al, 2006;Wong et al, 2007;Gao et al, 2008;Niehusmann et al, 2010). Spillover of glutamate as a result of inadequate reuptake, thereby activating extrasynaptic GluN2B subunits, seems crucial Wong et al, 2007).…”

Effect of chronic prenatal restraint stress on hippocampal neuronal cell density in male and female wistar rats at weaning

“…Gestational stress is reported to increase the anxiety like behavior in elevated plus maze or in open field (Kohman, et al 2008) and decrease the spatial learning and memory in T-maze (Son, et al 2006), diminution of time spent in target quadrant in the water maze, spontaneous alternation test in Y-maze (Darnaudéry 2006) and passive avoidance learning (Wu, et al 2007). Thus there are many instances in which neural function and cognition are either facilitated by prenatal stress (Yang, et al 2006) or even not affected (Schwalbe, et al 2010). Hence there is a paucity in prenatal stress and cognitive (sense of right and wrong) behavioral literature and the mechanisms underlying these lasting developmental and behavioral teratology.…”

Prenatal glucocorticoid exposure in rats: programming effects on stress reactivity and cognition in adult offspring

“…In rodents, prenatal stress programs hypersensitivity to stress, including heightened hypothalamicpituitary-adrenal (HPA) axis activity (Vallee et al, 1997;Wilson et al, 2013) and increased fear and anxiety-like behavior (Takahashi et al, 1992;Vallee et al, 1997;Wakshlak & Weinstock, 1990;Welberg et al, 2001). Prenatal stress also affects cognition as demonstrated by impaired spatial learning and memory (Brabham et al, 2000;Lemaire et al, 2000;Markham et al, 2010;Son et al, 2006;Yang et al, 2006), working memory (Gue et al, 2004;Markham et al, 2010) and cued and contextual fear conditioning and extinction (Green et al, 2011;Markham et al, 2010;Wilson et al, 2013). …”