Differential Effects of Corticosterone on the Slow Afterhyperpolarization in the Basolateral Amygdala and CA1 Region: Possible Role of Calcium Channel Subunits

Abstract

Liebmann L, Karst H, Sidiropoulou K, van Gemert N, Meijer OC, Poirazi P, Joëls M. Differential effects of corticosterone on the slow afterhyperpolarization in the basolateral amygdala and CA1 region: possible role of calcium channel subunits. J Neurophysiol 99: 958-968, 2008. First published December 12, 2007 doi:10.1152/jn.01137.2007. The stress hormone corticosterone increases the amplitude of the slow afterhyperpolarization (sAHP) in CA1 pyramidal neurons, without affecting resting membrane potential, input resistance, or action potential characteristics. We here examined how corticosterone affects these properties in the basolateral amygdala (BLA). In the amygdala, corticosterone does not change the AHP amplitude, nor any of the passive and active membrane properties studied. The lack of effect on the AHP is surprising since in both areas corticosterone increases highvoltage-activated sustained calcium currents, which supposedly regulate the sAHP. We wondered whether corticosterone targets different calcium channel subunits in the two areas because currents through only one of the subunits (Cav1.3) are thought to alter the AHP amplitude. In situ hybridization studies revealed that CA1 cells express Cav1.2 and Cav1.3 subunits; corticosterone does not transcriptionally regulate Cav1.2 but increases Cav1.3 expression compared with vehicle treatment. In the BLA, Cav1.3 expression was not detectable, both after control and corticosterone treatment. Cav1.2 is moderately expressed. In a modeling study, we examined putative consequences of changes in specific calcium channel subunit expression and calcium extrusion by corticosterone for the AHP in CA1 and amygdala neurons. A differential distribution and transcriptional regulation of Cav1.2 and Cav1.3 in the CA1 area versus BLA partly explain the observed differences in AHP amplitude. The functional implication of these findings could be that stress-induced arousal of activity in the BLA is more prolonged than that in the CA1 hippocampal area, so that information with an emotional component is more effectively encoded.

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

“…ing frequency accommodation and AHP) will not affect the likelihood of evoking a single spike upon depolarization but reduce the transfer of multiple spikes. High levels of corticosterone or glucocorticoids were found to enhance the amplitude of the I sAHP and AHP in CA1 pyramidal neurons, resulting in fewer spikes upon depolarization (Joëls and de Kloet, 1989;Kerr et al, 1989;Liebmann et al, 2008) (Fig. 8); this differs from the situation of predominant MR activation (such as occurs under rest), which is characterized by more spikes during a depolarizing pulse than in the absence of steroids (Joëls and de Kloet, 1990), reflecting the same U-shaped dose dependence as observed with respect to calcium current amplitude.…”

Glucocorticoids act on glutamatergic pathways to affect memory processes

“…Interestingly, in contrast to the transient effect observed in the CA1 area [21], the enhanced mEPSC activity in the amygdala is long lasting (i.e. maintained for several hours) [26], an effect that requires both rapidly induced MR-dependent [26] as well as delayed GR-dependent [27,28] enhancement of glutamatergic transmission.…”

Distinct Effects of Repeated Restraint Stress on Basolateral Amygdala Neuronal Membrane Properties in Resilient Adolescent and Adult Rats

“…Corticosterone increases the excitability of BA neurons and decreases mAHP amplitudes (3-5-week-old rats; Duvarci and Pare, 2007). However, the amplitude of the sAHP does not appear to be affected by single application of corticosterone (Liebmann et al, 2008). Corticosterone can also increase synaptic release of glutamate in the BLA in a rapid mineralocorticoid-dependent manner while decreasing glutamate release in a slow, glucocorticoid receptor-dependent manner (Karst et al, 2010).…”