Environmental Enrichment Differentially Activates Neural Circuits in FVB/N Mice, Inducing Social Interaction in Females but Agonistic Behavior in Males

Cabrera-Muñoz, Edith; Olvera-Hernández, Sandra; Vega‐Rivera, Nelly Maritza; Juan, David Meneses-San; Reyes‐Haro, Daniel; Ortíz-López, Leonardo; Ramírez-Rodríguez, Gerardo

doi:10.1007/s11064-021-03487-8

Cited by 6 publications

(3 citation statements)

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“…Firstly, out of all long-term in-space spatial complexity change interventions ( n = 19), most studies ( n = 14) combined the inclusion of running wheels with a change of in-cage complexity from once to five times per week, showing the effectiveness of a 1 to 3-month intervention in stimulating neurogenesis ( Kempermann et al, 1997 , 1998a , 1998b ; Nilsson et al, 1999 ; Segovia et al, 2006 ; Hattori et al, 2007 ; Ramírez-Rodríguez et al, 2014 ; Hosseiny et al, 2015 ; Zhang et al, 2016 ; Sadegzadeh et al, 2020 ; Sakhaie et al, 2020 ; Wang et al, 2020 ; Resasco et al, 2021 ; Cabrera-Muñoz et al, 2022 ). Regarding the remaining long-term in-space spatial complexity interventions, one study by Oatess et al (2021) investigated the effect of a single structural enrichment element (an acrylic tunnel), finding it was insufficient to affect hippocampal neurogenesis or markers of stress, two studies proved that a 6-month-long intervention for older subjects was effective with and without running wheels ( Freret et al, 2012 ; Neidl et al, 2016 ), a cohort study lasting 20 months demonstrated the effectiveness of the intervention in stimulating neurogenesis without running wheels and with the least frequency of changing in-cage complexity ( Birch and Kelly, 2019 ), and a 11-month-long intervention with combined running wheels and weekly changes in in-cage spatial complexity for 1-month-old subjects was effective in stimulating neurogenesis ( Hüttenrauch et al, 2016 ).…”

Section: Resultsmentioning

confidence: 99%

Environmental enrichment: a systematic review on the effect of a changing spatial complexity on hippocampal neurogenesis and plasticity in rodents, with considerations for translation to urban and built environments for humans

Khalil

2024

Front. Neurosci.

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IntroductionHippocampal neurogenesis is critical for improving learning, memory, and spatial navigation. Inhabiting and navigating spatial complexity is key to stimulating adult hippocampal neurogenesis (AHN) in rodents because they share similar hippocampal neuroplasticity characteristics with humans. AHN in humans has recently been found to persist until the tenth decade of life, but it declines with aging and is influenced by environmental enrichment. This systematic review investigated the impact of spatial complexity on neurogenesis and hippocampal plasticity in rodents, and discussed the translatability of these findings to human interventions.MethodsComprehensive searches were conducted on three databases in English: PubMed, Web of Science, and Scopus. All literature published until December 2023 was screened and assessed for eligibility. A total of 32 studies with original data were included, and the process is reported in accordance with the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) statement and checklist.ResultsThe studies evaluated various models of spatial complexity in rodents, including environmental enrichment, changes to in-cage elements, complex layouts, and navigational mazes featuring novelty and intermittent complexity. A regression equation was formulated to synthesize key factors influencing neurogenesis, such as duration, physical activity, frequency of changes, diversity of complexity, age, living space size, and temperature.ConclusionFindings underscore the cognitive benefits of spatial complexity interventions and inform future translational research from rodents to humans. Home-cage enrichment and models like the Hamlet complex maze and the Marlau cage offer insight into how architectural design and urban navigational complexity can impact neurogenesis in humans. In-space changing complexity, with and without physical activity, is effective for stimulating neurogenesis. While evidence on intermittent spatial complexity in humans is limited, data from the COVID-19 pandemic lockdowns provide preliminary evidence. Existing equations relating rodent and human ages may allow for the translation of enrichment protocol durations from rodents to humans.

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Section: Resultsmentioning

confidence: 99%

Environmental enrichment: a systematic review on the effect of a changing spatial complexity on hippocampal neurogenesis and plasticity in rodents, with considerations for translation to urban and built environments for humans

Khalil

2024

Front. Neurosci.

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“…Our study identified oligodendrocytes through the immunoreactivity of CNPase, a protein expressed during the transition from progenitor to differentiated oligodendrocytes. This protein has two different isoforms (short and long isoforms), which are differentially expressed during oligodendrocytes' formation [61,62]. Here, TMZ decreased the immunoreactivity of CNPase, but the decrement was prevented with the administration of MEL.…”

Section: Melatoninmentioning

confidence: 85%

Melatonin Prevents Depression but Not Anxiety-like Behavior Produced by the Chemotherapeutic Agent Temozolomide: Implication of Doublecortin Cells and Hilar Oligodendrocytes

Cabrera-Muñoz,

Ramírez-Rodríguez,

Díaz-Yañez

et al. 2023

IJMS

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Melatonin is a hormone synthesized by the pineal gland with neuroprotective and neurodevelopmental effects. Also, melatonin acts as an antidepressant by modulating the generation of new neurons in the dentate gyrus of the hippocampus. The positive effects of melatonin on behavior and neural development may suggest it is used for reverting stress but also for the alterations produced by chemotherapeutic drugs influencing behavior and brain plasticity. In this sense, temozolomide, an alkylating/anti-proliferating agent used in treating brain cancer, is associated with decreased cognitive functions and depression. We hypothesized that melatonin might prevent the effects of temozolomide on depression- and anxiety-like behavior by modulating some aspects of the neurogenic process in adult Balb/C mice. Mice were treated with temozolomide (25 mg/kg) for three days of two weeks, followed by melatonin (8 mg/kg) for fourteen days. Temozolomide produced short- and long-term decrements in cell proliferation (Ki67-positive cells: 54.89% and 53.38%, respectively) and intermediate stages of the neurogenic process (doublecortin-positive cells: 68.23% and 50.08%, respectively). However, melatonin prevented the long-term effects of temozolomide with the increased number of doublecortin-positive cells (47.21%) and the immunoreactivity of 2′ 3′-Cyclic-nucleotide-3 phosphodiesterase (CNPase: 82.66%), an enzyme expressed by mature oligodendrocytes, in the hilar portion of the dentate gyrus. The effects of melatonin in the temozolomide group occurred with decreased immobility in the forced swim test (45.55%) but not anxiety-like behavior. Thus, our results suggest that melatonin prevents the harmful effects of temozolomide by modulating doublecortin cells, hilar oligodendrocytes, and depression-like behavior tested in the forced swim test. Our study could point out melatonin’s beneficial effects for counteracting temozolomide’s side effects.

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“…Furthermore, another report has noted that EE had an anxiolytic effect on male mice but had the opposite effects in female mice based on results from the elevated T -maze test [ 241 ]. A recent study also found EE to differentially activate neural circuits in FVB/N mice, promoting social interactions in female mice but aggressive behaviors in male mice [ 242 ]. Additionally, many studies have also noted the sex-dependent effects of EE in their respective investigations [ 243 , 244 ].…”

Section: Discussion and Limitations Of Current Studiesmentioning

confidence: 99%

The Molecular Effects of Environmental Enrichment on Alzheimer’s Disease

2022

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Environmental enrichment (EE) is an environmental paradigm encompassing sensory, cognitive, and physical stimulation at a heightened level. Previous studies have reported the beneficial effects of EE in the brain, particularly in the hippocampus. EE improves cognitive function as well as ameliorates depressive and anxiety-like behaviors, making it a potentially effective neuroprotective strategy against neurodegenerative diseases such as Alzheimer’s disease (AD). Here, we summarize the current evidence for EE as a neuroprotective strategy as well as the potential molecular pathways that can explain the effects of EE from a biochemical perspective using animal models. The effectiveness of EE in enhancing brain activity against neurodegeneration is explored with a view to differences present in early and late life EE exposure, with its potential application in human being discussed. We discuss EE as one of the non pharmacological approaches in preventing or delaying the onset of AD for future research.

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Environmental Enrichment Differentially Activates Neural Circuits in FVB/N Mice, Inducing Social Interaction in Females but Agonistic Behavior in Males

Cited by 6 publications

References 65 publications

Environmental enrichment: a systematic review on the effect of a changing spatial complexity on hippocampal neurogenesis and plasticity in rodents, with considerations for translation to urban and built environments for humans

Environmental enrichment: a systematic review on the effect of a changing spatial complexity on hippocampal neurogenesis and plasticity in rodents, with considerations for translation to urban and built environments for humans

Melatonin Prevents Depression but Not Anxiety-like Behavior Produced by the Chemotherapeutic Agent Temozolomide: Implication of Doublecortin Cells and Hilar Oligodendrocytes

The Molecular Effects of Environmental Enrichment on Alzheimer’s Disease

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