Impairment of fear memory consolidation in maternally stressed male mouse offspring: Evidence for nongenomic glucocorticoid action on the amygdala

Eun Jeong Lee, Gi Hoon Son, Sooyoung Chung, Sukwon Lee, Jeongyeon Kim, Sukwoo Choi, Kyungjin Kim

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Abstract

The environment in early life elicits profound effects on fetal brain development that can extend into adulthood. However, the longlasting impact of maternal stress on emotional learning remains largely unknown. Here,wefocus on amygdala-related learning processes in maternally stressed mice. In these mice, fear memory consolidation and certain related signaling cascades were significantly impaired, though innate fear, fear memory acquisition, and synaptic NMDA receptor expression in the amygdala were unaltered. In accordance with these findings, maintenance of long-term potentiation (LTP) at amygdala synapses, but not its induction, was significantly impaired in the maternally stressed animals. Interestingly, amygdala glucocorticoid receptor expression was reduced in the maternally stressed mice, and administration of glucocorticoids (GCs) immediately after fear conditioning and LTP induction restored memory consolidation and LTP maintenance, respectively, suggesting that a weakening of GC signaling was responsible for the observed impairment. Furthermore, microinfusion of a membrane-impermeable form of GC (BSA-conjugated GC) into the amygdala mimicked the restorative effects of GC, indicating that a nongenomic activity of GC mediates the restorative effect. Together, these findings suggest that prenatal stress induces long-term dysregulation of nongenomic GC action in the amygdala of adult offspring, resulting in the impairment of fear memory consolidation. Since modulation of amygdala activity is known to alter the consolidation of emotionally influenced memories allocated in other brain regions, the nongenomic action of GC on the amygdala shown herein may also participate in the amygdala-dependent modulation of memory consolidation.

Original languageEnglish
Pages (from-to)7131-7140
Number of pages10
JournalJournal of Neuroscience
Volume31
Issue number19
DOIs
Publication statusPublished - 2011 May 11
Externally publishedYes

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ASJC Scopus subject areas

  • Neuroscience(all)

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