Antidepressive and BDNF effects of enriched environment treatment across ages in mice lacking BDNF expression through promoter IV

Jha, Shanker; Dong, Bo; Xue, Yi; Delotterie, David; Vail, Meghan G.; Sakata, Kazuko

doi:10.1038/tp.2016.160

Cited by 31 publications

(50 citation statements)

References 92 publications

(171 reference statements)

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“…In particular, EE protects from dendritic atrophy as well as reductions in neurogenesis and neurotrophin expression following adult stress (Hutchinson et al, 2012; Shilpa et al, 2017; Veena et al, 2009; Vega‐Rivera et al, 2016). Previous studies have also shown that exposure to EE during a critical developmental period (0–2 postnatal months), is more effective at increasing BDNF levels (Jha et al, 2016). In this respect, our BDNF increases are in line with existing evidence, indicating a beneficial role of post‐weaning EE (PND23‐65) against MS‐associated decreases in BDNF expression.…”

Section: Discussionmentioning

confidence: 96%

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

123

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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.

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Section: Discussionmentioning

confidence: 96%

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

123

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“…We found that EET effects in increasing exploratory activity and anti‐despair behavior were largest and long‐lasting when EET was provided during ED, particularly in promoter IV‐BDNF‐deficient mice . BDNF protein induction in the hippocampus and frontal cortex was also the largest after early‐life EET, while the EET effects were limited in old‐adult (OA) mice . These results led to our hypothesis that EET during ED provides maximum and lasting effects in antidepressive behavior and BDNF induction.…”

Section: Introductionmentioning

confidence: 89%

“…We recently examined EET effects across 3 distinctive life stages in mice: early‐life development (ED), young‐adulthood and old‐adulthood. We found that EET effects in increasing exploratory activity and anti‐despair behavior were largest and long‐lasting when EET was provided during ED, particularly in promoter IV‐BDNF‐deficient mice . BDNF protein induction in the hippocampus and frontal cortex was also the largest after early‐life EET, while the EET effects were limited in old‐adult (OA) mice .…”

Section: Introductionmentioning

confidence: 97%

The effect of enriched environment across ages: A study of anhedonia and BDNF gene induction

Dong

Xue

Sakata

2018

Genes Brain and Behavior

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Enriched environment treatment (EET) is a potential intervention for depression by inducing brain-derived neurotrophic factor (BDNF). However, its age dependency remains unclear. We recently found that EET during early-life development (ED) was effective in increasing exploratory activity and anti-despair behavior, particularly in promoter IV-driven BDNF deficient mice (KIV), with the largest BDNF protein induction in the hippocampus and frontal cortex. Here, we further determined age dependency of EET effects on anhedonia and promoter-specific BDNF transcription, by using the sucrose preference test and qRT-PCR. Wild-type (WT) and KIV mice received 2 months of EET during ED, young-adulthood and old-adulthood (0-2, 2-4 and 12-14 months, respectively). All KIV groups showed reduced sucrose preference, which EET equally reversed regardless of age. EET increased hippocampal BDNF mRNA levels for all ages and genotypes, but increased frontal cortex BDNF mRNA levels only in ED KIV and old WT mice. Transcription by promoters I and IV was age-dependent in the hippocampus of WT mice: more effective induction of exon IV or I during ED or old-adulthood, respectively. Transcription by almost all 9 promoters was age-specific in the frontal cortex, mostly observed in ED KIV mice. After discontinuance of EET, the EET effects on anti-anhedonia and BDNF transcription in both regions persisted only in ED KIV mice. These results suggested that EET was equally effective in reversing anhedonia and inducing hippocampal BDNF transcription, but was more effective during ED in inducing frontal cortex BDNF transcription and for lasting anti-anhedonic and BDNF effects particularly in promoter IV-BDNF deficiency.

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“…Early EE studies demonstrated widespread effects on numerous CNS cell types and under varied physiological conditions in both small and large mammals [84,85,86,87,88]. Differential rearing in infant rhesus monkey shows that animals raised in larger groups demonstrate expansion of the CC and sustained improvement in cognitive performance versus age-matched, individually raised controls [89].…”

Section: Environmentally Influenced Changes In Myelin Structure and Fmentioning

confidence: 99%

All Wrapped Up: Environmental Effects on Myelination

Forbes

Gallo

2017

Trends in Neurosciences

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Summary To date, studies have demonstrated the dynamic influence of exogenous environmental stimuli on multiple regions of the brain. This environmental influence positively and negatively impacts programs governing myelination, and acts on myelinating oligodendrocyte (OL) cells across the entire human lifespan. Developmentally, environmental manipulation of OL progenitor cells (OPCs) has profound effects on the establishment of functional cognitive, sensory, and motor programs. Furthermore, central nervous system (CNS) myelin remains an adaptive entity in adulthood, sensitive to environmentally induced structural changes. Here, we discuss the role of environmental stimuli on mechanisms governing programs of CNS myelination under normal and pathological conditions. Importantly, we highlight how these extrinsic cues can influence the intrinsic power of myelin plasticity to promote functional recovery.

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Antidepressive and BDNF effects of enriched environment treatment across ages in mice lacking BDNF expression through promoter IV

Cited by 31 publications

References 92 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

The effect of enriched environment across ages: A study of anhedonia and BDNF gene induction

All Wrapped Up: Environmental Effects on Myelination

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