Corticosterone time-dependently modulates β-adrenergic effects on long-term potentiation in the hippocampal dentate gyrus

Abstract

Previous experiments in the hippocampal CA1 area have shown that corticosterone can facilitate long-term potentiation (LTP) in a rapid non-genomic fashion, while the same hormone suppresses LTP that is induced several hours after hormone application. Here, we elaborated on this finding by examining whether corticosterone exerts opposite effects on LTP depending on the timing of hormone application in the dentate gyrus as well. Moreover, we tested rapid and delayed actions by corticosterone on ␤-adrenergic-dependent changes in LTP. Unlike the CA1 region, our in vitro field potential recordings show that rapid effects of corticosterone do not influence LTP induced by mild tetanization in the hippocampal dentate gyrus, unless GABA A receptors are blocked. In contrast, the ␤-adrenergic agonist isoproterenol does initiate a slow-onset, limited amount of potentiation. When corticosterone was applied concurrently with isoproterenol, a further enhancement of synaptic strength was identified, especially during the early stage of potentiation. Yet, treatment with corticosterone several hours in advance of isoproterenol fully prevented any effect of isoproterenol on LTP. This emphasizes that corticosterone can regulate ␤-adrenergic modulation of synaptic plasticity in opposite directions, depending on the timing of hormone application.

Severe Early Life Stress Hampers Spatial Learning and Neurogenesis, but Improves Hippocampal Synaptic Plasticity and Emotional Learning under High-Stress Conditions in Adulthood

“…Effects of maternal deprivation on synaptic plasticity in the dentate gyrus Low excitability of DG granule neurons in vitro is due to strong GABAergic inhibition and a hyperpolarized resting membrane potential (Wisden et al, 1992;Coulter and Carlson, 2007), making it difficult to induce LTP (Pu et al, 2007). Here, significant potentiation only occurred in the presence of the GABAergic antagonist bicuculline.…”

“…Sections containing the rostral part (Ϫ2.5 to Ϫ4.0 mm from bregma) (Paxinos and Watson, 1986) of the hippocampal dentate gyrus were placed in a recording chamber maintained at 30 -32°C with a constant flow of oxygenated aCSF. Field EPSPs (fEPSPs) were recorded as described previously (Pu et al, 2007;Bagot et al, 2009) in the absence or presence of the GABAergic antagonist bicuculline methiodide (10 M; Tebu-bio). fEPSPs were evoked using a stainless steel bipolar stimulation electrode (60 m diameter, insulated except for the tip) positioned in the medial perforant pathway and recorded through a glass electrode (2-5 M⍀ impedance, filled with aCSF) positioned in the middle third of the molecular layer of the upper blade.…”

β-Adrenergic facilitation of synaptic plasticity in the rat basolateral amygdala in vitro is gradually reversed by corticosterone

“…However, experiments in which the two hormones were not given concurrently showed that glucocorticoids may otherwise suppress the noradrenergic effect (Borrell et al 1984). This suggests that the interactive hormonal functions affecting the memory systems are not always uniform.Support for this nonuniformity was recently obtained in the hippocampal DG (Pu et al 2007). Corticosterone time-dependently modulated noradrenergic action on long-term potentiation (LTP), the best-described neurobiological substrate of learning and memory to date (Goosens and Maren 2002;Martin and Morris 2002;Morris 2003).…”

“…Corticosterone time-dependently modulated noradrenergic action on long-term potentiation (LTP), the best-described neurobiological substrate of learning and memory to date (Goosens and Maren 2002;Martin and Morris 2002;Morris 2003). Thus, b-adrenergic facilitation of LTP was accelerated if corticosterone was coapplied with the b-agonist isoproterenol, but suppressed if corticosterone was transiently applied several hours before the b-agonist (Pu et al 2007). In view of the behavioral observations that b-agonists and glucocorticoids both affect memory processes involving the BLA (Roozendaal et al 2002), we here investigated the time-dependent hormonal actions in this region.…”

“…The brain was removed from the skull and immersed in chilled buffer as previously described (Pu et al 2007); 500-mm-thick coronal slices containing the basolateral amygdala were made with a vibroslicer (Leica VT1000S). Slices were maintained in artificial cerebrospinal fluid (aCSF) (see Pu et al 2007) for >1 h before transfer to the recording chamber (30°C-32°C), where slices were kept submerged.The lateral amygdala (LA) supplies one of the major afferent pathways to the BLA (Pitkanen et al 1995;Wang et al 2002). A bipolar stimulation electrode (60 mm in diameter, stainless steel, insulated except for the tip) was placed in the LA to evoke field excitatory postsynaptic potentials in the BLA (glass microelectrodes, impedance 2-5 MV, filled with aCSF).…”