Environmental enrichment effects after early stress on behavior and functional brain networks in adult rats

González-Pardo, Héctor; Árias, Jorge L.; Vallejo, Guillermo; Conejo, Nélida M.

doi:10.1371/journal.pone.0226377

Cited by 33 publications

(26 citation statements)

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“…In this regard, impaired spatial learning and memory in male rats and deficits in behavioral flexibility in female rats have been associated with hippocampal and prefrontal cortex dysfunction after MS in rodents [ 35 , 37 , 55 ]. However, we found no significant effects of MS on brain CCO activity using a similar MS protocol in our previous study [ 34 ]. This discrepancy with our previous study could be due to multiple comparison errors and the small sample size used, since in this study, only males were analyzed and compared with additional groups reared under environmental enrichment conditions.…”

Section: Discussionmentioning

confidence: 45%

“…In particular, early MS during the two first weeks of life in rats seems to impair adult HPA axis response, because it overlaps with the ‘stress-hyporesponsive period’ (SHRP, PND 3-14 in rats) characterized by low ACTH and glucocorticoid levels in response to external stressors [ 7 , 32 ]. However, prolonged MS during the entire lactation period (PND 1-21) in rodents may have different effects on the HPA axis function during adulthood, as already reported regarding brain CCO activity [ 34 , 35 ]. Accordingly, increased brain CCO activity in MS female rats as compared to same-sex controls was reported using a short MS period (PND 1-10) that only partially overlapped the SHRP [ 35 ].…”

Section: Discussionmentioning

confidence: 94%

“…Given the paucity of studies about sex differences in the long-term effects of ELS on brain mitochondrial function, neurochemistry, and neuroinflammation, the present study aimed to evaluate these effects after prolonged MS in male and female rats over the entire weaning period (PND 1-21, 4 h/day) [ 34 , 35 , 36 , 37 , 38 , 39 ]. Evaluation of brain mitochondrial function was performed by quantification of regional brain oxidative metabolic capacity using cytochrome c oxidase (CCO) quantitative histochemistry.…”

Section: Introductionmentioning

confidence: 99%

“…Changes in brain CCO activity are directly coupled with changes in neuronal activity in order to meet its energy demands [ 40 ]. Quantitative CCO histochemistry in brain tissue has been applied in previous studies using several MS protocols in male or female rodents by our research group and others [ 32 , 34 , 35 , 41 ]. Brain oxidative capacity in selected regions of interest (prelimbic and infralimbic areas of the prefrontal cortex, cingulate cortex, dorsal and ventral hippocampus, and striatum) will be evaluated in adult (70-day-old) male and female rats after early prolonged MS as already described.…”

Section: Introductionmentioning

confidence: 99%

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Sex-Specific Effects of Early Life Stress on Brain Mitochondrial Function, Monoamine Levels and Neuroinflammation

et al. 2020

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Sex differences have been reported in the susceptibility to early life stress and its neurobiological correlates in humans and experimental animals. However, most of the current research with animal models of early stress has been performed mainly in males. In the present study, prolonged maternal separation (MS) paradigm was applied as an animal model to resemble the effects of adverse early experiences in male and female rats. Regional brain mitochondrial function, monoaminergic activity, and neuroinflammation were evaluated as adults. Mitochondrial energy metabolism was greatly decreased in MS females as compared with MS males in the prefrontal cortex, dorsal hippocampus, and the nucleus accumbens shell. In addition, MS males had lower serotonin levels and increased serotonin turnover in the prefrontal cortex and the hippocampus. However, MS females showed increased dopamine turnover in the prefrontal cortex and increased norepinephrine turnover in the striatum, but decreased dopamine turnover in the hippocampus. Sex differences were also found for pro-inflammatory cytokine levels, with increased levels of TNF-α and IL-6 in the prefrontal cortex and hippocampus of MS males, and increased IL-6 levels in the striatum of MS females. These results evidence the complex sex- and brain region-specific long-term consequences of early life stress.

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Section: Discussionmentioning

confidence: 45%

Section: Discussionmentioning

confidence: 94%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Sex-Specific Effects of Early Life Stress on Brain Mitochondrial Function, Monoamine Levels and Neuroinflammation

et al. 2020

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“…Several studies evaluating the effect of EE on brain development have observed increased neurogenesis, increase in dendritic ramifications, as well as increased nerve growth factor (NGF) gene expression and increased LTP in the hippocampus (19)(20)(21). EE has also been shown to improve learning and memory consolidation in animal models of Alzheimer's disease (22,23).…”

Section: Introductionmentioning

confidence: 99%

Environmental enrichment reverses memory impairment in B3-ARKO mice

Batistuzzo

et al. 2020

Preprint

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Norepinephrine plays an important role in modulating the processes of memory consolidation and evocation through its beta-adrenergic receptors (Adrβ), which are expressed in the hippocampus and amygdala. Several studies have shown that all three subtypes of Adrβ (β1, β2 and β3) play an important role in cognition. Environmental enrichment (EE), a technique initially used to decrease the stress of animals held in captive environments, has also been shown to produce cognitive benefits in both healthy and sick animals. In this study, we hypothesized that EE would reverse the memory impairment induced by the absence or Adrβ3. To test this, 21- and 86-day- old Adrβ3KO mice were exposed to an EE protocol for 8 weeks. The study showed that the EE protocol is able to correct the memory impairment when applied to Adrβ3KO animals immediately after weaning but has no effect when applied to adult animals. We also found that aging worsens the memory of Adrβ3KO mice. Our results suggest that a richer and more diverse environment helps to correct memory impairment in Adrβ3KO animals. They also reinforce the idea that noradrenergic signaling is involved in the cognitive impairment observed late in life, as aging led to a worsening in the memory of the Adrβ3KO animals that was not corrected by the environmental enrichment protocol. Key words: noradrenaline, cognitive benefits, memory, aging

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Environmental enrichment as a strategy: Attenuates the anxiety and memory impairment in social isolation stress

Keloğlan

Öztürk

Şahin

et al. 2022

Intl J of Devlp Neuroscience

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Background: Social isolation (SI) early in life produces behavioral and cognitive abnormalities. On the contrary, environmental enrichment (EE) offers beneficial effects on brain plasticity and development. This study was designed to examine how EE affects memory functions, anxiety level, and the expression levels of memory/anxiety-related genes such as NR2A, NR2B, BDNF, and cFos in the hippocampus of socially isolated rats.Materials and Methods: Wistar albino male rats (n = 40) were separated into the five groups: Standard cage (SC), SI, EE, SI + SC, and SI + EE group. For each group, eight rats were housed, either grouped or isolated, in a standard or 3-week EE, respectively. Morris water maze test (MWMT) was used for measuring the learning and memory function. Elevated plus maze (EPM) and open field (OF) were used for the evaluation of anxiety behavior. Blood corticosterone level was evaluated by the ELISA method. The expression levels of genes were measured by the RT-PCR method.Results: Results showed that EE increased memory performance in the SI group (p < 0.05). SI caused anxiety while EE improved anxiety behavior (p < 0.05). There was no significant difference between the groups in the OF test. Corticosterone levels did not change between groups. BDNF expression level was downregulated in EE and SI + SC compared with the SC group (respectively; p = 0.012; p = 0.011). NR2A, NR2B, and cFos expression levels did not change between groups significantly.Conclusions: SI impaired memory performance while EE has beneficial effects on memory in socially isolated rats. EE alone was insufficient to cause alterations in the memory performance. The therapeutic effects of EE became strengthened while applied together with stress protocol. Together with improving the effectiveness of memory function, EE has the potential to decrease anxiety behavior. EE seemed to be the reason for decreasing in BDNF.

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Environmental enrichment effects after early stress on behavior and functional brain networks in adult rats

Cited by 33 publications

References 96 publications

Sex-Specific Effects of Early Life Stress on Brain Mitochondrial Function, Monoamine Levels and Neuroinflammation

Sex-Specific Effects of Early Life Stress on Brain Mitochondrial Function, Monoamine Levels and Neuroinflammation

Environmental enrichment reverses memory impairment in B3-ARKO mice

Environmental enrichment as a strategy: Attenuates the anxiety and memory impairment in social isolation stress

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