Environmental enrichment enhances cognitive flexibility in C57BL/6 mice on a touchscreen reversal learning task

Zeleznikow-Johnston, Ariel M; Burrows, Emma L.; Renoir, Thibault; Hannan, Anthony J.

doi:10.1016/j.neuropharm.2017.02.009

Cited by 55 publications

(54 citation statements)

References 53 publications

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“…Among the main findings of this review, 17 of the 32 selected articles used male rats or mice (Amaral, Vargas, Hansel, Izquierdo, & Souza, ; Bechara & Kelly, ; Birch, McGarry, & Kelly, ; Eckert & Abraham, ; Faherty, Kerley, & Smeyne, ; Iso, Simoda, & Matsuyama, ; Kondo, Takei, & Hirokawa, ; Lerch, ; Madronal et al, ; Novkovic, Heumann, & Manahan‐Vaughan, ; Rizzi, Bianchi, Guidi, Ciani, & Bartesaghi, ; Silva, Duarte, Lima, & Oliveira, ; Vedovelli et al, ; Viola et al, ; Xu et al, ; Zeleznikow‐Johnston, Burrows, Renoir, & Hannan, ; Zhang et al, ), 8 evaluated only females (Fabel et al, ; Hosseiny et al, ; Kobilo et al, ; Nilsson, Perfilieva, Johansson, Orwar, & Eriksson, ; Prusky, Reidel, & Douglas, ; Valero‐Aracama, Sauvage, & Yoshida, ; Williams et al, ; Ziv et al, ), 1 article used male and female mice (Melani, Chelini, Cenni, & Berardi, ) and 6 did not identify the sex of the animals used in the study (Catlow et al, ; Huang, Huang, Wu, & Boucheron, ; Li, Niu, Jiang, & Hu, ; Rampon et al, ; Sampedro‐Piquero et al, ; Schloesser, Lehmann, Martinowich, Manji, & Herkenham, ).…”

Section: Resultsmentioning

confidence: 94%

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

Barros

David

Souza³

et al. 2019

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Background and aim: Environmental enrichment (EE) can be related to changes in the expression of brain-derived neurotrophic factor (BDNF) in the hippocampus of adult rodents. Exposure to EE may also induce neurogenesis in the dentate gyrus (DG). The aim of this systematic review was to analyze the current literature on the correlation between neurogenesis and BDNF expression in the hippocampal DG region resulting from exposure to EE, which is associated with changes in memory, in rodents. Methods:Bibliographic searches of the Medline/PubMed and ScienceDirect databases were carried out, and 334 studies were found. A predefined protocol was used and registered on PROSPERO, and 32 studies were included for qualitative synthesis. The PRISMA was used to report this systematic review. Results: Most of the included studies showed that there is little evidence in the literature demonstrating that memory changes resulting from EE are dependent on BDNF expression and that there is an induction of neurogenesis in the hippocampal DG. However, the observed increase in molecular expression levels and cell proliferation is dependent on the age, the timing and duration of exposure to EE. Regarding the methodological quality of the studies, the majority presented a risk of bias due to the high variability in the age of the animals. Conclusion: There are few studies in the literature that correlate the molecular and cellular mechanisms involved in neurogenesis in the hippocampal DG with BDNF expression in this region in rodents exposed to EE; however, there are other factors that can modulate this neurogenesis. K E Y W O R D Senvironmental enrichment, hippocampus, memory, neurogenesis

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Section: Resultsmentioning

confidence: 94%

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

Barros

David

Souza³

et al. 2019

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“…It is worth noting that those previous touchscreen studies were done using the “Med Associates” boxes, with sugar pellet rewards, whereas our study took place in the newly commercialized chambers (Cambden Instruments) with liquid rewards (i.e., strawberry milk), which may have influenced task difficulty (Horner et al, ; Oomen et al, ). Indeed, in the newly commercialized chambers, our group now routinely performs the Trial‐Unique Non‐Matching to Location task (Zeleznikow‐Johnston et al, ; Zeleznikow‐Johnston et al, ), a task that was deemed too difficult to be performed by mice in the previous generation of chambers (Oomen et al, ). Despite this, overall, our results show that exercise clearly affects cognitive flexibility in SERT HET mice, on both the MWM and the spatial pattern separation touchscreen task.…”

Section: Discussionmentioning

confidence: 99%

“…Mice then underwent pre‐training in the touchscreen chambers (~9 to 11 weeks of age) as exhaustively described elsewhere (Oomen et al, ). Strawberry milk (Strawberry Milk, Nippy's Ltd, Melbourne, Australia) was used as the reward (Zeleznikow‐Johnston, Burrows, Renoir, & Hannan, ). All testing occurred in the dark cycle, under red light, 6 days per week.…”

Section: Methodsmentioning

confidence: 99%

Paradoxical effects of exercise on hippocampal plasticity and cognition in mice with a heterozygous null mutation in the serotonin transporter gene

Rogers

Chen

Stanić

et al. 2019

British J Pharmacology

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Background and Purpose Exercise is known to improve cognitive function, but the exact synaptic and cellular mechanisms remain unclear. We investigated the potential role of the serotonin (5‐HT) transporter (SERT) in mediating these effects. Experimental Approach Hippocampal long‐term potentiation (LTP) and neurogenesis were measured in standard‐housed and exercising (wheel running) wild‐type (WT) and SERT heterozygous (HET) mice. We also assessed hippocampal‐dependent cognition using the Morris water maze (MWM) and a spatial pattern separation touchscreen task. Key Results SERT HET mice had impaired hippocampal LTP regardless of the housing conditions. Exercise increased hippocampal neurogenesis in WT mice. However, this was not observed in SERT HET animals, even though both genotypes used the running wheels to a similar extent. We also found that standard‐housed SERT HET mice displayed altered cognitive flexibility than WT littermate controls in the MWM reversal learning task. However, SERT HET mice no longer exhibited this phenotype after exercise. Cognitive changes, specific to SERT HET mice in the exercise condition, were also revealed on the touchscreen spatial pattern separation task, especially when the cognitive pattern separation load was at its highest. Conclusions and Implications Our study is the first evidence of reduced hippocampal LTP in SERT HET mice. We also show that functional SERT is required for exercise‐induced increase in adult neurogenesis. Paradoxically, exercise had a negative impact on hippocampal‐dependent cognitive tasks, especially in SERT HET mice. Taken together, our results suggest unique complex interactions between exercise and altered 5‐HT homeostasis.

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“…Numerous studies have shown that environmental enrichment (EE), a rodent analogue of rehabilitation, confers significant motor, cognitive, and histological benefits after experimental brain injury in both male and female rodents (Hamm et al, 1996; Passineau et al, 2001; Hicks et al, 2002; Kline et al, 2007; Sozda et al, 2010; de Witt et al, 2011; Bondi et al, 2014; Monaco et al, 2014; Radabaugh et al, 2016; Zeleznikow-Johnston et al, 2017). While the majority of the EE studies have focused on the traditional approach of providing enrichment early and continuously after brain injury, we have steadily been making significant strides in developing EE into a viable preclinical model of neurorehabilitation.…”

Section: Discussionmentioning

confidence: 99%

“…Clinically, this break in rehabilitation is to minimize fatigue so that effort does not wane. Experimentally, the renewed and robust interaction with the environment could lead to increased motor activity and a greater cognitive flexibility (De Bartolo et al, 2008; Zeleznikow-Johnston et al, 2017). …”

Section: Discussionmentioning

confidence: 99%

Refining environmental enrichment to advance rehabilitation based research after experimental traumatic brain injury

Radabaugh

LaPorte

Greene

et al. 2017

Experimental Neurology

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The typical environmental enrichment (EE) paradigm, which consists of continuous exposure after experimental traumatic brain injury (TBI), promotes behavioral and histological benefits. However, rehabilitation is often abbreviated in the clinic and administered in multiple daily sessions. While recent studies have demonstrated that a once daily 6-hr bout of EE confers benefits comparable to continuous EE, breaking the therapy into two shorter sessions may increase novelty and ultimately enhance recovery. Hence, the aim of the study was to test the hypothesis that functional and histological outcomes will be significantly improved by daily preclinical neurorehabilitation consisting of two 3-hr periods of EE vs. a single 6-hr session. Anesthetized adult male rats received a controlled cortical impact of moderate-to-severe injury (2.8 mm tissue deformation at 4m/s) or sham surgery and were then randomly assigned to groups receiving standard (STD) housing, a single 6-hr session of EE, or two 3-hr sessions of EE daily for 3 weeks. Motor function (beam-balance/traversal) and acquisition of spatial learning/memory retention (Morris water maze) were assessed on post-operative days 1–5 and 14–19, respectively. Cortical lesion volume was quantified on day 21. Both EE conditions improved motor function and acquisition of spatial learning, and reduced cortical lesion volume relative to STD housing (p < 0.05), but did not differ from one another in any endpoint (p > 0.05). The findings replicate previous work showing that 6-hr of EE daily is sufficient to confer behavioral and histological benefits after TBI and extend the findings by demonstrating that the benefits are comparable regardless of how the 6-hrs of EE are accrued. The relevance of the finding is that it can be extrapolated to the clinic and may benefit patients who cannot endure a single extended period of neurorehabilitation.

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Environmental enrichment enhances cognitive flexibility in C57BL/6 mice on a touchscreen reversal learning task

Cited by 55 publications

References 53 publications

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

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

Paradoxical effects of exercise on hippocampal plasticity and cognition in mice with a heterozygous null mutation in the serotonin transporter gene

Refining environmental enrichment to advance rehabilitation based research after experimental traumatic brain injury

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