Different types of environmental enrichment have discrepant effects on spatial memory and synaptophysin levels in female mice

Lambert, Talley J.; Fernandez, Stephanie M.; Frick, Karyn M.

doi:10.1016/j.nlm.2004.12.001

Cited by 164 publications

(125 citation statements)

References 66 publications

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“…Rats after acrobat training showed a mild increase (ϳ20%) in the number of Purkinje synapses in paramedian lobules (2). However, the acrobat-evoked synaptogenesis may predominantly occur in Purkinje cells, since the overall cerebellar level of synaptophysin (a synaptic vesicle fusion protein) in mice was unaltered by similar acrobat training (17). In our work, chronic treadmill running not only increased the synapse density in Purkinje cells (Fig.…”

Section: Discussionsupporting

confidence: 52%

Chronic treadmill exercise in rats delicately alters the Purkinje cell structure to improve motor performance and toxin resistance in the cerebellum

Huang

Lin

Cho

et al. 2012

Journal of Applied Physiology

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CJ. Chronic treadmill exercise in rats delicately alters the Purkinje cell structure to improve motor performance and toxin resistance in the cerebellum. J Appl Physiol 113: 889-895, 2012. First published July 26, 2012 doi:10.1152/japplphysiol.01363.2011.-Although exercise usually improves motor performance, the underlying cellular changes in the cerebellum remain to be elucidated. This study aimed to investigate whether and how chronic treadmill exercise in young rats induced Purkinje cell changes to improve motor performance and rendered the cerebellum less vulnerable to toxin insults. After 1-wk familiarization of treadmill running, 6-wk-old male Wistar rats were divided into exercise and sedentary groups. The exercise group was then subjected to 8 wk of exercise training at moderate intensity. The rotarod test was carried out to evaluate motor performance. Purkinje cells in cerebellar slices were visualized by lucifer yellow labeling in single neurons and by calbindin immunostaining in groups of neurons. Compared with sedentary control rats, exercised rats not only performed better in the rotarod task, but also showed finer Purkinje cell structure (higher dendritic volume and spine density with the same dendritic field). The exercise-improved cerebellar functions were further evaluated by monitoring the long-lasting effects of intraventricular application of OX7-saporin. In the sedentary group, OX7-saporin treatment retarded the rotarod performance and induced ϳ60% Purkinje cell loss in 3 wk. As a comparison, the exercise group showed much milder injuries in the cerebellum by the same toxin treatment. In conclusion, exercise training in young rats increased the dendritic density of Purkinje cells, which might play an important role in improving the motor performance. Furthermore, as Purkinje cells in the exercise group were relatively toxin resistant, the exercised rats showed good motor performance, even under toxin-treated conditions. morphology; OX7-saporin; two-photon microscopy; running; motor function THE RELATIONSHIP BETWEEN PHYSICAL activity and brain functions has been widely investigated. In particular, physical activity in older subjects benefits their mental health by protecting the brain against age-related deterioration (6). Many exercise studies primarily focus on brain structural and functional changes related to cognitive improvements (15), with relatively few studies focusing on the motor performance. Consequently, although connections between cognitive deficits and age-associated brain differences have been elucidated, relationships with motor performance are less well understood. Interestingly, aging impacts brain structures and associated behaviors differentially, with the cerebellum showing earlier senescence than the hippocampus (31). As physically active older adults require less error monitoring and show improvements in motor performance (26), it is desirable to explore the beneficial effects of exercise on the cerebellum. Purkinje cells in aged rats show pronounced dendrite degener...

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Section: Discussionsupporting

confidence: 52%

Chronic treadmill exercise in rats delicately alters the Purkinje cell structure to improve motor performance and toxin resistance in the cerebellum

Huang

Lin

Cho

et al. 2012

Journal of Applied Physiology

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“…Estrogen and enrichment influence similar aspects of hippocampal structure and function in young and aging female rodents, including spine density (Frick, Fernandez, Bennett, Prange-Kiel, MacLusky & Leranth, 2004;Miranda, Williams & Einstein, 1999;Rampon et al, 2000;Woolley & McEwen, 1992, neurogenesis (Kempermann et al, 1997(Kempermann et al, , 1998Tanapat, Hastings, Reeves & Gould, 1999), synaptophysin levels (Bennett et al, 2006;Frick & Fernandez, 2003;Frick et al, 2002;Lambert, Fernandez & Frick, 2005), long-term potentiation (Duffy et al, 2001;Foy et al, 1999;Warren et al, 1995), and growth factor levels Ickes et al, 2000;Pham et al, 1999). At this point, it is unclear which, if any, of these alterations might be related to the mnemonic changes seen in this study.…”

Section: Potential Neural Mechanismsmentioning

confidence: 70%

Life-long environmental enrichment differentially affects the mnemonic response to estrogen in young, middle-aged, and aged female mice

Gresack

Kerr

Frick

2007

Neurobiology of Learning and Memory

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The present study was designed to examine whether life-long exposure to standard or enriched housing affects the ability of estrogen to improve spatial and object memory throughout the lifespan. Three week-old female mice were maintained in standard or enriched housing up to and through ovariectomy and behavioral testing at 5, 17, or 22 months of age. Spatial memory was tested in the Morris water maze and object memory was tested using an object recognition task. Immediately after training each day, mice were injected intraperitoneally with vehicle or 0.2 mg/kg 17β-estradiol. Among young females, object recognition was enhanced by estradiol alone, an effect that was reduced by enrichment. In contrast, spatial water maze performance was impaired by estradiol alone, but improved by the combination of both estradiol and enrichment. At middle-age, object recognition was enhanced by estradiol or enrichment alone, and the combination of both treatments. Spatial memory in the water maze was also improved by both treatments at middle-age, but the beneficial effects of estradiol were limited to standard-housed females. Finally, whereas enrichment in aged females significantly enhanced performance in both tasks, estradiol had no effect at this age in either task. In total, the data indicate that life-long enrichment can significantly alter the extent to which estradiol affects memory in mice throughout the lifespan. Importantly, the interaction between these treatments is highly dependent on age and type of memory tested.

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“…In rats, enrichment without wheel running has been shown to have anxiolytic effects upon exposure to an inescapable foot shock procedure and result in altered monoamine metabolism (Hendriksen et al 2010). Enrichment only also has effects on synaptic plasticity, such as increased dendritic complexity of young granule neurons (Beauquis et al 2010), enhanced arborization of cortical neurons (Ip et al 2002), and elevated synaptophysin levels in hippocampus and cortex (Lambert et al 2005). Thus, environmental enrichment and physical activity share common features pertaining to synaptic plasticity (van Praag et al 2000;Will et al 2004).…”

mentioning

confidence: 99%

Running is the neurogenic and neurotrophic stimulus in environmental enrichment

Kobilo¹,

Liu²,

Gandhi³

et al. 2011

Learn. Mem.

332

253

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Environmental enrichment (EE) increases dentate gyrus (DG) neurogenesis and brain-derived neurotrophic factor (BDNF) levels. However, running is considered an element of EE. To dissociate effects of physical activity and enrichment on hippocampal neurogenesis and BDNF levels, young female C57Bl/6 mice were housed under control, running, enrichment, or enrichment plus running conditions, and injected with bromodeoxyuridine. Cell genesis was assessed after 12 d and differentiation was analyzed 1 mo later. In addition, locomotor activity in the open field and hippocampal mature BDNF peptide levels were measured. Open-field adaptation was improved in all groups, compared to controls, but more so with running. New cell proliferation, survival, neuron number, and neurotrophin levels were enhanced only when running was accessible. We conclude that exercise is the critical factor mediating increased BDNF levels and adult hippocampal neurogenesis.[Supplemental material is available for this article.]Exposure to environmental enrichment (EE) has positive effects on brain function, including increased numbers of dendritic branches and spines, enlargement of synapses, and improved cognition (Bennett et al. 1964;Rosenzweig and Bennett 1996). More recently, it was discovered that EE enhances the survival of newly born neurons in the dentate gyrus (DG) of the hippocampus (Kempermann et al. 1997) and increases brain-derived neurotrophic factor (BDNF) levels (Falkenberg et al. 1992;Rossi et al. 2006;Sun et al. 2010). EE has many aspects, including increased opportunity for learning, socialization, and physical activity. Among these, exercise was found to enhance neurogenesis (van Praag et al. 1999). Subsequently, physical activity and enrichment have been regarded as equivalent neurogenic stimuli, albeit with different underlying mechanisms. Exercise is considered to mainly enhance cell proliferation, whereas enrichment is deemed to increase new cell survival (Olson et al. 2006;Kempermann et al. 2010). However, in many studies the enriched environment includes physical activity (Kempermann et al. 1997(Kempermann et al. , 1998van Praag et al. 1999;Rossi et al. 2006;Schloesser et al. 2010;Sun et al. 2010), making it difficult to assess the unique contributions of EE and exercise to adult neurogenesis, neurotrophin levels, and behavior.The current study aims to directly differentiate between the effects of enriched environment only (EEO), physical activity (RUN), and the combination of enrichment and running (EER). Here we show that running is the critical factor in stimulating adult hippocampal neurogenesis and enhancing mature BDNF peptide levels. Moreover, enrichment in the absence of running does not increase adult hippocampal neurogenesis or BDNF levels in the hippocampus. Open-field adaptation was improved in all groups as compared to controls, but more so in the groups that included running. These findings suggest that enrichment and exercise are distinct functional interventions.Forty female C57B1/6 mice (5 wk old) were div...

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Different types of environmental enrichment have discrepant effects on spatial memory and synaptophysin levels in female mice

Cited by 164 publications

References 66 publications

Chronic treadmill exercise in rats delicately alters the Purkinje cell structure to improve motor performance and toxin resistance in the cerebellum

Chronic treadmill exercise in rats delicately alters the Purkinje cell structure to improve motor performance and toxin resistance in the cerebellum

Life-long environmental enrichment differentially affects the mnemonic response to estrogen in young, middle-aged, and aged female mice

Running is the neurogenic and neurotrophic stimulus in environmental enrichment

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