Can the effects of environmental enrichment modulate BDNF expression in hippocampal plasticity? A systematic review of animal studies

Barros, Waleska Maria Almeida; David, Mírian Celly Medeiros Miranda; Souza, Ariani Impieri de; Silva, Mariluce; Matos, Rhowena Jane Barbosa de

doi:10.1002/syn.22103

Cited by 20 publications

(8 citation statements)

References 82 publications

(226 reference statements)

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“…Altogether, our findings suggest that, as compared with CEE, REE recruited the BDNF-TrkB signaling to a greater and broader extent. Although brain and behavioral data corresponded to independent experiments, changes in that signaling pathway may have underlain the behavioral improvements seen in the REE group, as it has been shown with protocols of continuous EE (Bekinschtein et al, 2011;Chourbaji et al, 2011; for a review see Barros et al, 2019).…”

Section: Experiments 2 Ree Alters Gene Expression In the Hippocampus Amentioning

confidence: 92%

“…EE induces numerous physiological, structural, cellular, synaptic, and molecular adaptations, especially in the hippocampus and the mesocorticolimbic circuits (Bekinschtein et al, 2011;Barros et al, 2019;Ohline and Abraham, 2019). Such adaptations comprise changes in signaling pathways and the expression of several genes underlying the neurobehavioral effects of EE (Simpson and Kelly, 2011;Zhang et al, 2018;Ohline and Abraham, 2019).…”

Section: Experiments 2 Ree Alters Gene Expression In the Hippocampus Amentioning

confidence: 99%

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Neurobehavioral Effects of Restricted and Unpredictable Environmental Enrichment in Rats

2020

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To study how motivational factors modulate experience-dependent neurobehavioral plasticity, we modify a protocol of environmental enrichment (EE) in rats. We assumed that the benefits derived from EE might vary according to the level of incentive salience attributed to it. To enhance the rewarding properties of EE, access to the EE cage varied randomly from 2 to 48 h for 30 days (REE). The REE group was enriched only 50% of the time and was compared to standard housing and continuous EE (CEE) groups. As behavioral readout, we analyzed the spontaneous activity and the ultrasonic vocalizations (USVs) within the EE cage weekly, and in the open field test at the end of the experiment. In the cage, REE increased the utilization of materials, physical activity, and the rate of appetitive USVs. In the OF, the CEE-induced enhancements in novelty habituation and social signaling were equaled by the REE. At the neural level, we measured the expression of genes related to neural plasticity and epigenetic regulations in different brain regions. In the dorsal striatum and hippocampus, REE upregulated the expression of the brainderived neurotrophic factor, its tropomyosin kinase B receptor, and the DNA methyltransferase 3A. Altogether, our results suggest that the higher activity within the cage and the augmented incentive motivation provoked by the REE boosted its neurobehavioral effects equaling or surpassing those observed in the CEE condition. As constant exposures to treatments or stimulating environments are virtually impossible for humans, restricted EE protocols would have greater translational value than traditional ones.

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Section: Experiments 2 Ree Alters Gene Expression In the Hippocampus Amentioning

confidence: 92%

Section: Experiments 2 Ree Alters Gene Expression In the Hippocampus Amentioning

confidence: 99%

Neurobehavioral Effects of Restricted and Unpredictable Environmental Enrichment in Rats

2020

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“…EE is a prominent method of improving general wellbeing and rescuing stress-induced behavioural deficits in adult animals 75 . EE also enhances AHN in adult animals [76][77][78][79] . Based on this literature, we may predict that EE during adolescence would be similarly beneficial for AHN and hippocampal-dependent behaviour.…”

Section: Discussionmentioning

confidence: 94%

Environmental enrichment rescues survival and function of adult-born neurons following early life stress

et al. 2020

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Adverse experiences early in life are associated with the development of psychiatric illnesses. The hippocampus is likely to play pivotal role in generating these effects: it undergoes significant development during childhood and is extremely reactive to stress. In rodent models, stress in the prepubertal period impairs adult hippocampal neurogenesis (AHN) and behaviours which rely on this process. In normal adult animals, environmental enrichment (EE) is a potent promoter of AHN and hippocampal function. Whether exposure to EE during adolescence can restore normal hippocampal function and AHN following pre-pubertal stress (PPS) is unknown. We investigated EE as a treatment for reduced AHN and hippocampal function following PPS in a rodent model. Stress was administered between post-natal days (PND) 25-27, EE from PND35 to early adulthood, when behavioural testing and assessment of AHN took place. PPS enhanced fear reactions to a CS following a trace fear protocol and reduced the survival of 4-week-old adult-born neurons throughout the adult hippocampus. Furthermore, we show that fewer adult-born neurons were active during recall of the CS stimulus following PPS. All effects were reversed by EE. Our results demonstrate lasting effects of PPS on the hippocampus and highlight the utility of EE during adolescence for restoring normal hippocampal function. EE during adolescence is a promising method of enhancing impaired hippocampal function resulting from early life stress, and due to multiple benefits (low cost, few side effects, widespread availability), should be more thoroughly explored as a treatment option in human sufferers of childhood adversity.

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“…Other studies also show that rats and mice submitted to EE present improvement in learning and memory, as well as better performance in cognitive tasks when compared to rodents kept in standard cages. In addition, they also have increased levels of brainderived neurotrophic factor (BDNF) and NGF, particularly in the hippocampus region, indicating neuronal growth and proliferation, and brain plasticity (36)(37)(38). Thus, it is likely that the improvement in memory tasks observed in young Adrβ3KO mice submitted to EE can be explained by these changes in neurotrophin expression.…”

Section: Discussionmentioning

confidence: 99%

Environmental enrichment reverses memory impairment in B3-ARKO mice

Batistuzzo

et al. 2020

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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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Can the effects of environmental enrichment modulate BDNF expression in hippocampal plasticity? A systematic review of animal studies

Cited by 20 publications

References 82 publications

Neurobehavioral Effects of Restricted and Unpredictable Environmental Enrichment in Rats

Neurobehavioral Effects of Restricted and Unpredictable Environmental Enrichment in Rats

Environmental enrichment rescues survival and function of adult-born neurons following early life stress

Environmental enrichment reverses memory impairment in B3-ARKO mice

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