Activity and plasticity in the CA1, the dentate gyrus, and the amygdala following controllable vs. uncontrollable water stress

The level of controllability has been shown to modulate the effects of stress on physiology and behavior. In the present study, we investigated the effects of controllable vs. uncontrollable stressors on plasticity in hippocampal CA1, the dentate gyrus (DG), and basal amygdala nucleus (B) in the rat, using the electrophysiological procedure of long-term potentiation (LTP). A naive group was left undisturbed until the electrophysiological recording commenced. Rats of the two controllable stress groups were trained in the Morris water maze to locate an invisible underwater platform (the first group), or visible platform (the second group), thus escaping from the water, before the recording. The uncontrollable stress group underwent the same procedure (exposure time to water was adjusted to the averaged exposure time of the first controllable group) without the escape platform. We first assessed the effects of stress and controllability on LTP in CA1. Both controllable stressors and the uncontrollable stress impaired CA1 LTP, with a more robust effect induced by the uncontrollable stress. We further assessed the effects of the same procedures on LTP in DG and B. The uncontrollable stress enhanced LTP in DG and increased baseline responses (suggesting uncontrollable stress-induced plasticity) in the amygdala. All the stressors decreased amygdalar LTP. An assessment of plasma levels of corticosterone (CORT), following the behavioral procedures, revealed an enhancement in CORT release following the uncontrollable, but not controllable stress, indicating the uncontrollable condition as the most stressful. These findings provide insight into the differential effects of stress and stress controllability on different hippocampal subregions and the amygdala.