Purkinje Cell Dendritic Atrophy Induced by Prenatal Stress Is Mitigated by Early Environmental Enrichment

Pascual, Rodrigo; Valencia, Martina; Bustamante, Carlos

doi:10.1055/s-0034-1395344

Cited by 9 publications

(9 citation statements)

References 35 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…In fact, existing evidence indicates that EE attenuates the chronic stress impact on behavior and hippocampal integrity, thus protecting against the stress-associated cognitive deficits, emotional dysregulation, dendritic atrophy and reduced neurogenesis (Hutchinson et al, 2012;Veena et al, 2009;Wright and Conrad, 2008). Similar to adult stress, restorative effects of EE have been reported in rodents submitted to prenatal (Laviola et al, 2008;Pascual et al, 2015;Yang et al, 2007) or juvenile stress (Ilin and Richter-Levin, 2009). To the best of our knowledge, there is limited information regarding the compensatory action of EE following early stress (do Prado et al, 2016;Francis et al, 2002;Koe et al, 2016;Vivinetto et al, 2013) and so far, no study has looked at the interaction of maternal separation and subsequent exposure to EE conditions concurrently at cognitive and emotional behavior, HPA function and markers of synaptic plasticity (BDNF, SYN) during adulthood.…”

Section: Introductionmentioning

confidence: 99%

Beneficial effects of environmental enrichment on behavior, stress reactivity and synaptophysin/BDNF expression in hippocampus following early life stress

Dandi

Kalamari

Touloumi

et al. 2018

Intl J of Devlp Neuroscience

120

View full text Add to dashboard Cite

Exposure to environmental enrichment can beneficially influence the behavior and enhance synaptic plasticity. The aim of the present study was to investigate the mediated effects of environmental enrichment on postnatal stress-associated impact with regard to behavior, stress reactivity as well as synaptic plasticity changes in the dorsal hippocampus. Wistar rat pups were submitted to a 3 h maternal separation (MS) protocol during postnatal days 1-21, while another group was left undisturbed. On postnatal day 23, a subgroup from each rearing condition (maternal separation, no-maternal separation) was housed in enriched environmental conditions until postnatal day 65 (6 weeks duration). At approximately three months of age, adult rats underwent behavioral testing to evaluate anxiety (Elevated Plus Maze), locomotion (Open Field Test), spatial learning and memory (Morris Water Maze) as well as non-spatial recognition memory (Novel Object Recognition Test). After completion of behavioral testing, blood samples were taken for evaluation of stress-induced plasma corticosterone using an enzyme-linked immunosorbent assay (ELISA), while immunofluorescence was applied to evaluate hippocampal BDNF and synaptophysin expression in dorsal hippocampus. We found that environmental enrichment protected against the effects of maternal separation as indicated by the lower anxiety levels and the reversal of spatial memory deficits compared to animals housed in standard conditions. These changes were associated with increased BDNF and synaptophysin expression in the hippocampus. Regarding the neuroendocrine response to stress, while exposure to an acute stressor potentiated corticosterone increases in maternally-separated rats, environmental enrichment of these rats prevented this effect. The current study aimed at investigating the compensatory role of enriched environment against the negative outcomes of adverse experiences early in life concurrently on emotional and cognitive behaviors, HPA function and neuroplasticity markers.

show abstract

Section: Introductionmentioning

confidence: 99%

Beneficial effects of environmental enrichment on behavior, stress reactivity and synaptophysin/BDNF expression in hippocampus following early life stress

Dandi

Kalamari

Touloumi

et al. 2018

Intl J of Devlp Neuroscience

120

View full text Add to dashboard Cite

show abstract

“…In relation to enrichment, post-weaning EE in male and female mice enhanced social preference, reduced anxiety-like behaviors, and improved spatial learning in adulthood (Hendershott et al, 2016 ; Aujnarain et al, 2018 ). As well, when housed in an EE with their siblings after weaning, male offspring born to dams stressed during pregnancy had reduced anxiety-like behaviors and limited Purkinje cell dendritic atrophy over the life course (Pascual et al, 2015 ). Thus, it is possible that the negative effects of social enrichment in male mice could be avoided by placing mice in EE immediately after weaning as opposed to early adulthood.…”

Section: Introductionmentioning

confidence: 99%

Post-weaning Environmental Enrichment in Male CD-1 Mice: Impact on Social Behaviors, Corticosterone Levels and Prefrontal Cytokine Expression in Adulthood

McQuaid

Dunn

Jacobson‐Pick

et al. 2018

Front. Behav. Neurosci.

View full text Add to dashboard Cite

Environmental enrichment is typically associated with enhanced well-being, improved cognitive function and stress resilience. However, in some instances grouping adult male mice in enriched conditions promoted a stressful environment, which resulted in elevated endocrine, monoamine and inflammatory outcomes in response to subsequent stressor exposure. The current investigation examined whether raising male mice in an enriched environment (EE) would modulate social and anxiety-like behaviors in early adulthood and influence brain expression of pro-inflammatory cytokines and brain-derived neurotrophic factor (BDNF). Immediately after weaning (postnatal day [PD] 21), CD-1 male mice were housed with their siblings (3/cage) for 6 weeks in an EE or a standard (SE) environment. Body weights and aggressive interactions were monitored weekly. Social avoidance behaviors in the social interaction test and anxiety-like behaviors in the elevated-plus maze were examined in early adulthood. Ninety minutes following the behavioral tests, mice were sacrificed and a blood sample and the prefrontal cortex (PFC) were collected for the determination of plasma corticosterone levels as well as cytokine and BDNF mRNA expression. Mice raised in an EE exhibited more wounds and gained less weight than mice housed in a SE. Enriched mice also spent a greater amount of time in proximity of a social target in the social interaction test and made fewer transitions into the closed arms of the elevated-plus maze. Interestingly, the elevated plasma corticosterone and upregulated prefrontal interleukin (IL)-1β expression observed after the social interaction test among the SE mice were not apparent among those housed in an EE. Enrichment also increased prefrontal BDNF expression, especially among mice that experienced the social interaction test. These results suggest that although raising male mice in an EE may elicit aggressive interactions between sibling cage-mates (as indicated by a high number of wounds), this environment also enhances social behaviors and limits the corticosterone and cytokine impacts of mild social stressors encountered in early adulthood.

show abstract

“…For example, exposing rodents to an enriched environment (EE) with rich social and sensorimotor stimulation decreased anxiety-like behaviours in an elevated plus maze11121314, improved sensorimotor skills1516 and led to larger cell proliferation and neuronal density17 along with increased expression of brain-derived neurotrophic factor (BDNF)1819. In prenatally stressed F1 offspring, EE decreases anxiety-like and fear behaviours14, improves social behaviour20, restores dendritic and synaptic morphology2122 and rescues density of glucocorticoid receptors23. Here we aim to determine if EE represents an effective therapy for the endocrine and behavioural consequences of epigenetically inherited manifestations of transgenerational stress in rats.…”

mentioning

confidence: 99%

Environmental Intervention as a Therapy for Adverse Programming by Ancestral Stress

McCreary

Erickson

Hao

et al. 2016

Sci Rep

View full text Add to dashboard Cite

Ancestral stress can program stress sensitivity and health trajectories across multiple generations. While ancestral stress is uncontrollable to the filial generations, it is critical to identify therapies that overcome transgenerational programming. Here we report that prenatal stress in rats generates a transgenerationally heritable endocrine and epigenetic footprint and elevated stress sensitivity which can be alleviated by beneficial experiences in later life. Ancestral stress led to downregulated glucocorticoid receptor and prefrontal cortex neuronal densities along with precocious development of anxiety-like behaviours. Environmental enrichment (EE) during adolescence mitigated endocrine and neuronal markers of stress and improved miR-182 expression linked to brain-derived neurotrophic factor (BDNF) and neurotrophin-3 (NT-3) regulation in stressed lineages. Thus, EE may serve as a powerful intervention for adverse transgenerational programming through microRNA-mediated regulation of BDNF and NT-3 pathways. The identification of microRNAs that mediate the actions of EE highlights new therapeutic strategies for mental health conditions and psychiatric disease.

show abstract

Purkinje Cell Dendritic Atrophy Induced by Prenatal Stress Is Mitigated by Early Environmental Enrichment

Abstract: Our data show that long-lasting Purkinje cell dendritic impairments and anxiety-like behavior can be mitigated by postweaning EE.

Cited by 9 publications

References 35 publications

Beneficial effects of environmental enrichment on behavior, stress reactivity and synaptophysin/BDNF expression in hippocampus following early life stress

Beneficial effects of environmental enrichment on behavior, stress reactivity and synaptophysin/BDNF expression in hippocampus following early life stress

Post-weaning Environmental Enrichment in Male CD-1 Mice: Impact on Social Behaviors, Corticosterone Levels and Prefrontal Cytokine Expression in Adulthood

Environmental Intervention as a Therapy for Adverse Programming by Ancestral Stress

Contact Info

Product

Resources

About