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

Abstract

The rat basolateral amygdala is important for emotional learning; this is modulated by noradrenaline and corticosterone. We report that the b-adrenergic agonist isoproterenol markedly enhances synaptic plasticity induced in the basolateral amygdala by a weak stimulation paradigm but is ineffective with stronger protocols. Simultaneous application of corticosterone gradually reversed the facilitatory effect of isoproterenol. When corticosterone was briefly applied several hours prior to isoproterenol, facilitatory effects of the b-agonist were entirely suppressed. This suggests that in the basolateral amygdala, b-adrenergic influences promote synaptic plasticity; this is gradually normalized by corticosterone, preventing the network from overshooting.The amygdala is crucially involved in the modulation of emotional memory (Cahill and McGaugh 1998;LeDoux 2000;McGaugh 2004;Richter-Levin 2004), as clearly demonstrated in the animal model of fear conditioning (LeDoux et al. 1990;Romanski et al. 1993;Rogan et al. 1997;Nader et al. 2001;Blair et al. 2003). It was also proposed that the amygdala-that is, the basolateral nucleus (BLA)-can modulate memory-related processes in other brain regions, e.g., the hippocampus (McGaugh et al. 1996;Akirav and Richter-Levin 2002;Kim and Diamond 2002;Pare 2003; RichterLevin and Akirav 2003;Roozendaal 2003;Richter-Levin 2004;Roozendaal et al. 2006a); thus, memory traces constructed in the hippocampus that are ''emotionally tagged'' have a competitive advantage for retention (Richter-Levin and Akirav 2003;Diamond et al. 2005;Vouimba et al. 2007).Within the BLA, multiple neuromodulatory systems influence memory, including the noradrenergic and glucocorticoid systems (Quirarte et al. 1997;Roozendaal 2003;Roozendaal et al. 2006a). Animal behavioral studies suggested that noradrenergic activity within the BLA plays a central role in mediating a memoryenhancing effect, while glucocortoid receptor (GR) activation exerts a ''permissive'' function (Roozendaal et al. 2002(Roozendaal et al. , 2006b). 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). 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...

Time-Dependent Effects of Corticosteroids on Human Amygdala Processing

“…Corticosteroids have been shown to act in such direct manner in the hippocampus, where they rapidly increase neuronal excitability in a nongenomic fashion by binding to a low-affinity membrane MR (Karst et al, 2005;Olijslagers et al, 2008) and slowly impair hippocampal function by binding intracellular MRs and GRs. Corticosteroids could affect amygdala function in a similar manner, but supporting evidence for this idea is so far scarce (Karst et al, 2002;Duvarci and Pare, 2007;Pu et al, 2009). Alternatively, the corticosteroid effects might be mediated by a reduction in brain levels of corticotrophin-releasing hormone (CRH).…”

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

“…There are indeed several examples of noradrenaline and corticosterone acting in concert to promote optimal neural function (Akirav and Richter-Levin, 2002; Korz and Frey, 2005;Zhou et al, 2011), which is also reflected at the behavioral level (Roozendaal et al, 2004). Yet when corticosterone is given Ͼ1 h in advance of noradrenaline or isoproterenol, the hormone suppresses noradrenergic function (Joëls and de Kloet, 1989;Pu et al, 2007Pu et al, , 2009Liebmann et al, 2009). This is possibly caused by occlusion because the two compounds converge on the same functional endpoints, which would be another example of metaplastic changes induced by corticosteroids; right now this is pure speculation.…”

“…At both the single-cell and the field-potential levels, corticosterone did not quickly change AMPA or NMDA receptor-mediated synaptic responses (Liebmann et al, 2009;Pu et al, 2009).…”

Location and Function of the Slow Afterhyperpolarization Channels in the Basolateral Amygdala

“…In BLA projection neurons, the sI AHP is suppressed by muscarinic (Washburn and Moises, 1992b;Power and Sah, 2008), ␤-adrenergic Power and Sah, 2008), and metabotropic glutamatergic (Womble and Moises, 1994) receptor activation. Activation of these transmitter systems facilitates the induction of long-term potentiation (LTP) (Watanabe et al, 1995;Huang and Kandel, 1996;Ferry et al, 1997;Fendt and Schmid, 2002;Rodrigues et al, 2002;Pu et al, 2009). However, the actions of these transmitter systems are not limited to their suppression of the sI AHP , and thus such correlative data do not provide a causative link between the sI AHP and synaptic plasticity.…”