Effects of environmental enrichment on anxiety responses, spatial memory and cytochrome c oxidase activity in adult rats

Sampedro-Piquero, Patricia; Zancada-Menendez, C.; Begega, Azucena; Rubio, Sandra; Árias, Jorge L.

doi:10.1016/j.brainresbull.2013.06.006

Cited by 44 publications

(38 citation statements)

References 61 publications

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“…A literature search indicated that energy metabolism-related proteins were decreased in positively stimulating conditions, while they increased in stressful conditions or mental disorders [31,32,33,34]. In support of our results, two interesting studies showed that a lower level of brain activation was observed in EE animals following an anxiety-inducing task [35,36]. The current proteomic study provides supportive evidence for a qualitatively different metabolic response seen in EE.…”

Section: Discussionsupporting

confidence: 79%

Alteration of Energy Metabolism and Antioxidative Processing in the Hippocampus of Rats Reared in Long-Term Environmental Enrichment

Kang

Choi²,

Kim³

et al. 2016

Dev Neurosci

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Environmental enrichment (EE) is a typical experimental method that promotes levels of novelty and complexity that enhance experience-dependent neuroplasticity and cognitive behavior function in laboratory animals. Early EE is associated with resilience in the face of later-life challenges. Since increased synaptic activity enhances endogenous neuronal antioxidant defenses, we hypothesized that long-term EE beginning at an early stage may alter the levels of oxidative stress. We investigated global protein expression and oxidative stress in hippocampal proteins from rats nurtured for a 6-month EE beginning in the prenatal period. The analysis of protein expression was carried out using 2-dimensional gel electrophoresis with matrix-associated laser desorption ionization time-of-flight mass spectrometry. Proteins with altered expression were involved in energy metabolism (phosphoglycerate mutase 1, α-enolase isoform 1, adenylate kinase 1, and triose phosphate isomerase) and antioxidant enzymes (superoxide dismutase 1, glutathione S-transferase ω type 1, peroxiredoxin 5, DJ-1, and glial maturation factor β). Using Western blot assays, some of the proteins with altered expression and NADPH oxidase 2 were confirmed to be decreased. Further confirmation was demonstrated with attenuated expression of 7,8-dihydro-8-oxo-deoxyguanine, a DNA oxidative stress marker, in the hippocampus of EE group rats. Our data demonstrate that a long-term EE program beginning in the prenatal and early postnatal phase of development modulates energy metabolism and reduced oxidant stress possibly through enhanced synaptic activity. We provide evidence that EE can be developed as a tool to protect the brain from oxidative stress-induced injury.

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Section: Discussionsupporting

confidence: 79%

Alteration of Energy Metabolism and Antioxidative Processing in the Hippocampus of Rats Reared in Long-Term Environmental Enrichment

Kang

Choi²,

Kim³

et al. 2016

Dev Neurosci

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“…Although it is believed that subjects who present low trait anxiety experience state anxiety reactions less frequently, and with smaller intensity, than individuals with high trait anxiety levels [9], it has already been demonstrated that, in animal models, this correlation is not necessarily true [17,24]. On the other hand, a recent study demonstrated that adult rats kept in EE for eight weeks presented lower levels of anxiety in the elevated zero-maze (EZM), in comparison to animals maintained in standard cages [25]. EZM is an animal model derived from EPM and very similar to it in terms of detecting anxiolytic and anxiogenic drug effects in rats [26].…”

Section: Resultsmentioning

confidence: 98%

Environmental enrichment for adult rats: Effects on trait and state anxiety

Goes

Antunes

Teixeira-Silva

2015

Neuroscience Letters

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Experimental evidence indicates that enriched environment (EE) induces neurobiological and behavioural alterations. EE in early life improves learning and memory and reduces trait and state anxiety. However, the effect of EE established in adulthood has rarely been investigated. Thus, the aim of this study was to evaluate the possibility of modifying the levels of trait and/or state anxiety of adult rats exposed to EE. Seventy adult Wistar male rats were first tested in the free-exploratory paradigm (FEP) and were categorized according to their levels of trait anxiety (high, medium and low). Subsequently, half of the animals from each category returned to their home cages (standard condition: SC) and the other half was transferred to an enriched environment (enriched condition: EC). After three weeks, all animals were again tested in FEP. Seven to 10 days later, fifty of the seventy animals were tested on the elevated plus-maze test (EPM). In FEP, EE reduced locomotor activity in the second exposition independently of the anxiety category and, it decreased the levels of trait anxiety of highly anxious rats. No effect of EE was observed on EPM. In conclusion, EE established in adulthood was able to reduce high trait anxiety, a major risk factor for anxiety disorders.

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“…Relevant effects of EE exposure on the amygdala include alterations in expression of corticotropin releasing factor receptors (Sztainberg, Kuperman, Tsoory, Lebow, & Chen, 2010), increased proliferation of progenitor cells and suppressed apoptosis (Okuda et al, 2009), increased brain-derived neurotropic factor levels (Segovia, Del Arco, de Blas, Garrido, & Mora, 2008), and increased gastrin-releasing peptide receptors, which are involved in fear learning (Qian, Zhou, Pan, Liu, & Wang, 2008). EE exposure also produces alterations in the PFC such as increased energy metabolism as assessed by cytochrome c oxidase histochemistry (Sampedro-Piquero et al, 2013), increased FosB immunostaining (Lehmann & Herkenham, 2011), and increased concentrations of serotonin (Brenes, Rodriguez, & Fornaguera, 2008). Future research will be necessary to determine the anatomical and neurochemical basis for the effects of EE on extinction.…”

Section: Discussionmentioning

confidence: 98%

“…A variety of alterations have been observed in the hippocampus, including increased neurogenesis (Kempermann, Kuhn, & Gage, 1997), enhanced long-term potentiation (Duffy, Craddock, Abel, & Nguyen, 2001;Green & Greenough, 1986), increased synaptic density (Rampon et al, 2000), and enhanced arborization of dendrites (Leggio et al, 2005). More recent work has indicated that EE can alter neurobiological variables in a number of brain areas including structures known for their role in fear conditioning and extinction such as the amygdala (Okuda et al, 2009) andprefrontal cortex (Sampedro-Piquero, ZancadaMenendez, Begega, Rubio, &Arias, 2013).…”

Section: Introductionmentioning

confidence: 95%

“…Rats reared in an EE demonstrate enhanced performance in the Morris water maze (Kempermann et al, 1997;Nilsson, Perfilieva, Johansson, Orwar, & Eriksson, 1999), radial arm maze (Leggio et al, 2005), radial arm water maze (Sampedro-Piquero et al, 2013), contextual fear conditioning (Rampon et al, 2000) and novel object recognition memory task (Birch, McGarry, & Kelly, 2013). However, the effects of EE exposure are not limited to hippocampal-dependent tasks.…”

Section: Introductionmentioning

confidence: 98%

See 1 more Smart Citation

Impaired extinction of fear conditioning after REM deprivation is magnified by rearing in an enriched environment

Hunter

2015

Neurobiology of Learning and Memory

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Effects of environmental enrichment on anxiety responses, spatial memory and cytochrome c oxidase activity in adult rats

Cited by 44 publications

References 61 publications

Alteration of Energy Metabolism and Antioxidative Processing in the Hippocampus of Rats Reared in Long-Term Environmental Enrichment

Alteration of Energy Metabolism and Antioxidative Processing in the Hippocampus of Rats Reared in Long-Term Environmental Enrichment

Environmental enrichment for adult rats: Effects on trait and state anxiety

Impaired extinction of fear conditioning after REM deprivation is magnified by rearing in an enriched environment

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