An Effect of Chronic Stress on Prospective Memory via Alteration of Resting-State Hippocampal Subregion Functional Connectivity

Chen, Jierong; Wei, Zhen; Han, Hongying; Jin, Lili; Xu, Chuanyong; Dong, Dan; Lu, Jianping; Wan, Guobin; Peng, Ziwen · 2019 · OpenAlex-citations

DOI: 10.1038/s41598-019-56111-9

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Summary

This study investigates the neural mechanisms underlying the impairment of prospective memory (PM) caused by chronic stress, specifically focusing on alterations in the functional connectivity (FC) of hippocampal subregions. While chronic stress is known to impair higher-order cognitive functions via hypothalamic-pituitary-adrenocortical axis activation and glucocorticoid release, the specific effects on hippocampal subregion networks related to PM remained unclear. The researchers hypothesized that chronic stress would lower PM performance and selectively alter the FC of hippocampal subregions, which would correlate with these performance deficits. The study employed a longitudinal design with 21 college students who underwent assessments at two time points: a baseline period one month prior to final examinations and a chronic stress period during the examination week. Participants completed event-based (EBPM) and time-based (TBPM) prospective memory tasks using a dual-task paradigm, alongside resting-state functional magnetic resonance imaging (fMRI). Stress levels were quantified using the Student-Life Stress Inventory (SLSI). Hippocampal subregions—Cornu ammonis 1 (CA1), Cornu ammonis 2, 3 and dentate gyrus (CA23DG), and the subicular complex (SUBC)—were identified using the Anatomy Toolbox in SPM12. Seed-based FC analysis compared connectivity patterns between baseline and stress conditions, controlling for motion and physiological noise. Results indicated that chronic stress significantly increased SLSI scores and decreased performance in both EBPM and TBPM, with TBPM showing a greater decline. Neuroimaging data revealed distinct subregion-specific changes: the FC of CA23DG with the bilateral caudate and precuneus increased under stress, whereas the FC of SUBC with the left middle frontal gyrus, left inferior parietal gyrus, and right supramarginal gyrus decreased. No significant changes were observed in the CA1 network. Crucially, these connectivity changes correlated with PM deficits. Increased CA23DG-caudate FC was negatively correlated with EBPM performance, while decreased SUBC-left inferior parietal gyrus FC was negatively correlated with both EBPM and TBPM performance. The findings suggest that chronic stress impairs prospective memory through specific alterations in hippocampal subregion networks. The increased connectivity of CA23DG, a region involved in coding new associations, with the caudate may reflect maladaptive processing of affective stimuli, while the decreased connectivity of SUBC, involved in retrieving learned associations, with parietal regions likely disrupts the maintenance of future intentions. These results provide evidence for a functional dissociation within the hippocampus during stress, identifying altered subregion-specific FC as a key mechanism for stress-induced cognitive impairment.

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• prospective memory interruptions