Dissociation of dorsal hippocampal regional activation under the influence of stress in freely behaving rats

Abstract

Stress has deleterious effects on brain, body, and behavior in humans and animals alike. The present work investigated how 30-min acute photic stress exposure impacts on spatial information processing in the main sub-regions of the dorsal hippocampal formation [CA1, CA3, and dentate gyrus (DG)], a brain structure prominently implicated in memory and spatial representation. Recordings were performed from spatially tuned hippocampal and DG cells in rats while animals foraged in a square arena for food. The stress procedure induced a decrease in firing frequencies in CA1 and CA3 place cells while sparing locational characteristics. In contrast to the CA1-CA3 network, acute stress failed to induce major changes in the DG neuronal population. These data demonstrate a clear dissociation of the effects of stress on the main hippocampal sub-regions. Our findings further support the notion of decreased hippocampal excitability arising from behavioral stress in areas CA1 and CA3, but not in DG.

Keywords: CA1; CA3; dentate gyrus; freely moving; hippocampus; place cells; stress.

Figure 1

Schematic drawings of the implantation sites; cells were recorded from pyramidal cell layers of the hippocampus, in particular, CA1, CA3, and the granule cell layer of the DG. Dotted lines represent the dense neuronal layers of each structure. The gray shaded areas represent the main granule cell layer of the dentate gyrus.

Figure 2

Summary of the effects of acute photic stress on CA1, CA3, and DG cells; CA1 and CA3 cells generally experience a significant decrease in firing activity whereas spatial characteristics are mainly unchanged. In contrast, DG cells do not experience a change in firing rate after stress. Black bars represent mean sample values of control sessions and gray bars represent mean sample values of stress sessions. The size of place fields was defined by the firing frequency above 20% of the maximum firing frequency. In total 99 cell pairs (control/stress) were recorded. n_CA1 = 34, n_CA3 = 18, n_DG = 47 *p < 0.05, **p < 0.01, ^‡Spatial information content in bits per spike.

Figure 3

Examples of firing characteristics of hippocampal and subicular neurons. The first column of each subregion depicts the smoothed color coded map showing the firing rate per pixel scaled to the maximum firing rate within the environment at the top left. Dark blue denotes the lowest firing category and red indicates the highest firing category. Color steps are in 20% of the maximum firing rate. The second column shows the corresponding path trajectories and the corresponding spikes of the neurons in red. The third column depicts the cell signal of the most prominent channel where time is plotted on the x-axis and spike amplitude is plotted on the y-axis. Two consecutive rows always show the same cell in both the control (firing rate in red) and stress condition (black).

Figure 4

Comparison between neuronal firing frequency changes. Maximum and average firing frequency changes of cells between two consecutive control sessions, as well as one control session and a successive stress session. *p < 0.05, **p < 0.01.