Differential Modulation of Long-Term Depression by Acute Stress in the Rat Dorsal and Ventral Hippocampus

Abstract

The ventral hippocampus (VH) was recently shown to express lower-magnitude long-term potentiation (LTP) than the dorsal hippocampus (DH). An exposure to acute stress reversed this difference, and VH slices from stressed rats expressed larger LTP than controls, whereas LTP in the DH was suppressed by stress. We have now used long-term depression (LTD)-generating trains of stimulation to examine whether this differential LTP reflects a genuine difference in synaptic modifiability between the two sectors of the hippocampus. Surprisingly, slices of DH and VH express similar magnitudes of LTD. However, while prior stress enhanced LTD in the DH, it actually converted LTD to slow-onset, robust LTP in the VH. These two effects of stress on LTD were blocked by glucocorticosterone receptor (GR) and mineralocorticosterone receptor (MR) antagonists, respectively. Acute exposure of slices to a GR agonist dexamethasone facilitated LTD in slices of both DH and VH, while activation of MRs by aldosterone converted LTD to LTP in both regions. Thus, differential activation of the two species of corticosterone receptors determines the ability of the two sectors of the hippocampus to undergo plastic changes in response to LTD-inducing stimulation.

Glucocorticoid actions on synapses, circuits, and behavior: Implications for the energetics of stress

“…Upon corticosterone application, the ventral hippocampus has reduced firing frequency accommodation and more depolarization-associated spikes (Maggio and Segal, 2009a). Further, unlike CA1, stress does not lead to impaired LTP in the ventral subiculum (Maggio and Segal, 2010, 2009b, 2007). These differential effects in the ventral hippocampus may allow for a longer window of acquisition when this brain region is activated during a stressful experience (Joëls et al, 2012).…”

The adaptive and maladaptive continuum of stress responses – a hippocampal perspective

“…Exposure to chronic or acute uncontrollable or intense stressors (chronic social defeat, inescapable shock, CUS or exposure to mixed restraint and swim stress) impairs induction of LTP in the Schaffer collateral-CA1 pathway (Kim et al, 1996;Ryan et al, 2010;Liu et al, 2012), commissural/associational input to the CA3 (Pavlides et al, 2002;Chen et al, 2010b), mossy fiber-CA3 synapses (Takeda et al, 2009;Chen et al, 2010a) and the medial perforant pathway to the DG (Pavlides et al, 2002). The stress-evoked impairment in LTP is noted to be more pronounced in the dorsal hippocampus, which plays a pivotal role in learning and memory, rather than the ventral hippocampus which is implicated in emotional processing (Maggio and Segal, 2009). These stress-evoked LTP deficits are fairly long-lasting and are noted up to 4 weeks following cessation of stressor experience (Ryan et al, 2010).…”

High-frequency stimulation-induced synaptic potentiation in dorsal and ventral CA1 hippocampal synapses: the involvement of NMDA receptors, mGluR5, and (L-type) voltage-gated calcium channels

“…Remarkably, this ability is not uniformly distributed along the long axis of the structure. Namely, the ability for longterm potentiation (LTP) induced by high-frequency stimulation (HFS) is strikingly lower in the ventral hippocampus (VH) compared with the dorsal hippocampus (DH) (Papatheodoropoulos and Kostopoulos 2000;Maruki et al 2001;Colgin et al 2004;Maggio and Segal 2009;Kenney and Manahan-Vaughan 2013;Keralapurath et al 2014). This is one of the most notable differences recently found in the intrinsic circuitry between the DH and the VH.…”