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Early maternal deprivation affects dentate gyrus structure and emotional learning in adult female rats.

Oomen CA, Soeters H, Audureau N, Vermunt L, van Hasselt FN, Manders EM, Joëls M, Krugers H, Lucassen PJ - Psychopharmacology (Berl.) (2010)

Bottom Line: No effects on the rate of adult neurogenesis were found.Furthermore, MD did not alter synaptic plasticity in vitro, neither under normal nor high-stress conditions.Although early life stress exposure did not impair hippocampus-dependent functioning in female offspring, it irreversibly affected DG structure by reducing cell numbers.

View Article: PubMed Central - PubMed

Affiliation: Swammerdam Institute for Life Sciences, Center for Neuroscience, University of Amsterdam, Amsterdam, The Netherlands. c.a.oomen@uva.nl

ABSTRACT

Rationale: Stress elicits functional and structural changes in the hippocampus. Early life stress is one of the major risk factors for stress-related pathologies like depression. Patients suffering from depression show a reduced hippocampal volume, and in women, this occurs more often when depression is preceded by childhood trauma. However, the underlying mechanisms that account for a reduced hippocampal volume are unknown.

Objective: We examined the effects of maternal absence on structure and function of the hippocampus in female offspring.

Methods: We studied whether 24 h of maternal deprivation (MD) on postnatal day 3 altered adult neurogenesis, individual neuronal morphology and dentate gyrus (DG) structure in young adult female rats. In addition, functional alterations were addressed by studying synaptic plasticity in vitro, and spatial as well as emotional learning was tested.

Results: Adult females that were subjected to MD revealed significant reductions in DG granule cell number and density. In addition, DG neurons were altered in their dendritic arrangement. No effects on the rate of adult neurogenesis were found. Furthermore, MD did not alter synaptic plasticity in vitro, neither under normal nor high-stress conditions. In addition, spatial learning and contextual fear conditioning were comparable between control and MD animals. However, MD animals showed an improved amygdala-dependent fear memory.

Conclusion: Although early life stress exposure did not impair hippocampus-dependent functioning in female offspring, it irreversibly affected DG structure by reducing cell numbers. This may be relevant for the reduced hippocampal volume observed in depression and the increased vulnerability of women to develop depression.

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Related in: MedlinePlus

Effects of MD on synaptic plasticity. a LTP measured under vehicle conditions (CON n = 7, MD n = 7). There was no effect of maternal deprivation on the degree of LTP in the dentate gyrus after theta burst stimulation (CON vs. MD; F1,28 = 0.03; p = 0.86) when comparing the second half of baseline recordings (t = −10 to 0 min) with post-TBS recordings. b Long-term potentiation after acute corticosterone application. The degree of LTP was not affected by corticosterone application, and there was no difference between CON (n = 7) and MD (n = 7) animals (F1,28 = 0.04; p = 0.84), interaction group × treatment (F1,28 = 0.002; p = 0.96)
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Fig2: Effects of MD on synaptic plasticity. a LTP measured under vehicle conditions (CON n = 7, MD n = 7). There was no effect of maternal deprivation on the degree of LTP in the dentate gyrus after theta burst stimulation (CON vs. MD; F1,28 = 0.03; p = 0.86) when comparing the second half of baseline recordings (t = −10 to 0 min) with post-TBS recordings. b Long-term potentiation after acute corticosterone application. The degree of LTP was not affected by corticosterone application, and there was no difference between CON (n = 7) and MD (n = 7) animals (F1,28 = 0.04; p = 0.84), interaction group × treatment (F1,28 = 0.002; p = 0.96)

Mentions: The effects of corticosterone on the degree of LTP was determined by perfusion of 100 nM corticosterone during the second half of baseline recordings, co-terminating with the end of TBS. Corticosterone application in itself had no effect on the magnitude of the signal during the second half of baseline recordings, as revealed by a repeated measures ANOVA comparing baseline 1 (t = −20 to −11 min) with baseline 2 (t = −10 to 0 min; baseline × drug × group, F1,28 = 2.3, p = 0.14; drug × group, F1,28 = 2.4, p = 0.14). For LTP, no significant effects were found on the degree of potentiation of group (CON vs. MD; F1,28 = 0.03; p = 0.86) and drug treatment (F1,28 = 0.04; p = 0.84), nor an interaction effect between these two (F1,28 = 0.002; p = 0.96), when comparing the second half of baseline recordings (t = −10 to 0 min) with post-TBS recordings (t = 0–60 min; Fig. 2a, b).Fig. 2


Early maternal deprivation affects dentate gyrus structure and emotional learning in adult female rats.

Oomen CA, Soeters H, Audureau N, Vermunt L, van Hasselt FN, Manders EM, Joëls M, Krugers H, Lucassen PJ - Psychopharmacology (Berl.) (2010)

Effects of MD on synaptic plasticity. a LTP measured under vehicle conditions (CON n = 7, MD n = 7). There was no effect of maternal deprivation on the degree of LTP in the dentate gyrus after theta burst stimulation (CON vs. MD; F1,28 = 0.03; p = 0.86) when comparing the second half of baseline recordings (t = −10 to 0 min) with post-TBS recordings. b Long-term potentiation after acute corticosterone application. The degree of LTP was not affected by corticosterone application, and there was no difference between CON (n = 7) and MD (n = 7) animals (F1,28 = 0.04; p = 0.84), interaction group × treatment (F1,28 = 0.002; p = 0.96)
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3045507&req=5

Fig2: Effects of MD on synaptic plasticity. a LTP measured under vehicle conditions (CON n = 7, MD n = 7). There was no effect of maternal deprivation on the degree of LTP in the dentate gyrus after theta burst stimulation (CON vs. MD; F1,28 = 0.03; p = 0.86) when comparing the second half of baseline recordings (t = −10 to 0 min) with post-TBS recordings. b Long-term potentiation after acute corticosterone application. The degree of LTP was not affected by corticosterone application, and there was no difference between CON (n = 7) and MD (n = 7) animals (F1,28 = 0.04; p = 0.84), interaction group × treatment (F1,28 = 0.002; p = 0.96)
Mentions: The effects of corticosterone on the degree of LTP was determined by perfusion of 100 nM corticosterone during the second half of baseline recordings, co-terminating with the end of TBS. Corticosterone application in itself had no effect on the magnitude of the signal during the second half of baseline recordings, as revealed by a repeated measures ANOVA comparing baseline 1 (t = −20 to −11 min) with baseline 2 (t = −10 to 0 min; baseline × drug × group, F1,28 = 2.3, p = 0.14; drug × group, F1,28 = 2.4, p = 0.14). For LTP, no significant effects were found on the degree of potentiation of group (CON vs. MD; F1,28 = 0.03; p = 0.86) and drug treatment (F1,28 = 0.04; p = 0.84), nor an interaction effect between these two (F1,28 = 0.002; p = 0.96), when comparing the second half of baseline recordings (t = −10 to 0 min) with post-TBS recordings (t = 0–60 min; Fig. 2a, b).Fig. 2

Bottom Line: No effects on the rate of adult neurogenesis were found.Furthermore, MD did not alter synaptic plasticity in vitro, neither under normal nor high-stress conditions.Although early life stress exposure did not impair hippocampus-dependent functioning in female offspring, it irreversibly affected DG structure by reducing cell numbers.

View Article: PubMed Central - PubMed

Affiliation: Swammerdam Institute for Life Sciences, Center for Neuroscience, University of Amsterdam, Amsterdam, The Netherlands. c.a.oomen@uva.nl

ABSTRACT

Rationale: Stress elicits functional and structural changes in the hippocampus. Early life stress is one of the major risk factors for stress-related pathologies like depression. Patients suffering from depression show a reduced hippocampal volume, and in women, this occurs more often when depression is preceded by childhood trauma. However, the underlying mechanisms that account for a reduced hippocampal volume are unknown.

Objective: We examined the effects of maternal absence on structure and function of the hippocampus in female offspring.

Methods: We studied whether 24 h of maternal deprivation (MD) on postnatal day 3 altered adult neurogenesis, individual neuronal morphology and dentate gyrus (DG) structure in young adult female rats. In addition, functional alterations were addressed by studying synaptic plasticity in vitro, and spatial as well as emotional learning was tested.

Results: Adult females that were subjected to MD revealed significant reductions in DG granule cell number and density. In addition, DG neurons were altered in their dendritic arrangement. No effects on the rate of adult neurogenesis were found. Furthermore, MD did not alter synaptic plasticity in vitro, neither under normal nor high-stress conditions. In addition, spatial learning and contextual fear conditioning were comparable between control and MD animals. However, MD animals showed an improved amygdala-dependent fear memory.

Conclusion: Although early life stress exposure did not impair hippocampus-dependent functioning in female offspring, it irreversibly affected DG structure by reducing cell numbers. This may be relevant for the reduced hippocampal volume observed in depression and the increased vulnerability of women to develop depression.

Show MeSH
Related in: MedlinePlus