Environmental enrichment promotes improved spatial abilities and enhanced dendritic growth in the rat

Leggio, Maria; Mandolesi, Laura; Federico, Francesca; Spirito, Francesca; Ricci, Benedetta; Gelfo, Francesca; Petrosini, Laura

doi:10.1016/j.bbr.2005.04.009

Cited by 441 publications

(319 citation statements)

References 79 publications

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“…However, no improvement in learning or memory was observed in EE WT mice, potentially due to the degree of difficulty of the tasks used and ceiling effects in performance. EE has been shown to have notable effects on structural plasticity in WT animals, including increasing dendritic branching and length, number of dendritic spines, and size of synapses (Faherty et al, 2003;Greenough and Volkmar, 1973;Leggio et al, 2005). In the present study, WT animals raised in environmentally enriched conditions show subtle alterations in dendritic complexity; however, spine density was unchanged.…”

Section: Discussionmentioning

confidence: 38%

Environmental Enrichment Ameliorates Behavioral Impairments Modeling Schizophrenia in Mice Lacking Metabotropic Glutamate Receptor 5

Burrows

McOmish

Buret

et al. 2015

Neuropsychopharmacol

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Schizophrenia arises from a complex interplay between genetic and environmental factors. Abnormalities in glutamatergic signaling have been proposed to underlie the emergence of symptoms, in light of various lines of evidence, including the psychotomimetic effects of NMDA receptor antagonists. Metabotropic glutamate receptor 5 (mGlu5) has also been implicated in the disorder, and has been shown to physically interact with NMDA receptors. To clarify the role of mGlu5-dependent behavioral expression by environmental factors, we assessed mGlu5 knockout (KO) mice after exposure to environmental enrichment (EE) or reared under standard conditions. The mGlu5 KO mice showed reduced prepulse inhibition (PPI), long-term memory deficits, and spontaneous locomotor hyperactivity, which were all attenuated by EE. Examining the cellular impact of genetic and environmental manipulation, we show that EE significantly increased pyramidal cell dendritic branching and BDNF protein levels in the hippocampus of wild-type mice; however, mGlu5 KO mice were resistant to these alterations, suggesting that mGlu5 is critical to these responses. A selective effect of EE on the behavioral response to the NMDA receptor antagonist MK-801 in mGlu5 KO mice was seen. MK-801-induced hyperlocomotion was further potentiated in enriched mGlu5 KO mice and treatment with MK-801 reinstated PPI disruption in EE mGlu5 KO mice only, a response that is absent under standard housing conditions. Together, these results demonstrate an important role for mGlu5 in environmental modulation of schizophreniarelated behavioral impairments. Furthermore, this role of the mGlu5 receptor is mediated by interaction with NMDA receptor function, which may inform development of novel therapeutics.

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Section: Discussionmentioning

confidence: 38%

Environmental Enrichment Ameliorates Behavioral Impairments Modeling Schizophrenia in Mice Lacking Metabotropic Glutamate Receptor 5

Burrows

McOmish

Buret

et al. 2015

Neuropsychopharmacol

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“…Morgan 1973;Renner and Rozenzweig 1987). Conversely, enrichment has been shown to improve the performance of rats in spatial cognitive tasks (Williams et al 2001;Schrijver et al 2002;Frick and Fernandez 2003;Leggio et al 2005). Various authors have suggested that these eVects of environmental enrichment on spatial memory may be mediated through alterations in hippocampal functioning, promoting hippocampal neurogenesis and dendritic branching and reducing apoptosis (Kempermann et al 1997;Young et al 1999;Meshi et al 2006;Bindu et al 2007; see also Olson et al 2006 for a review).…”

Section: Introductionmentioning

confidence: 99%

Spatial learning in pigs: effects of environmental enrichment and individual characteristics on behaviour and performance

et al. 2008

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This study investigated the eVects of both environmental enrichment and individual behavioural characteristics on spatial cognitive capabilities of pigs, using a novel latent spatial learning paradigm based on Tolman's detour experiments (1948). Pigs were housed either in 'barren' pens or in pens enriched with straw bedding from birth. Pigs were restrained in a Backtest at 10 and 17 days postpartum. Based on their escape behaviour in this test, which has been shown to reXect their behavioural style, six 'high-resisting'(HR) and six 'low-resisting' (LR) pigs were selected from each housing environment (n = 24 in total). At 12 weeks of age, pairs of pen mates (LR and HR) were exposed to a maze three times (exploration trials). Pigs were then placed individually in the maze, and social reinstatement proved to be a strong incentive to Wnd the exit leading to the home pen. We subsequently blocked the direct route to the exit, forcing animals to Wnd a detour (memory test 1, MT1). This test was repeated once to investigate the relative improvement, i.e. detour learning (memory test 2, MT2). Housing condition and Backtest response strongly aVected exploration patterns. In spite of this, no eVects on performance during the subsequent memory tests were found. Performance was substantially improved in MT2, indicating that once a goal is apparent, pigs are able to solve a complex spatial memory task easily. In conclusion, social reinstatement provided a good incentive to complete a spatial task, and the substantial improvement in performance between MT1 and MT2 stresses the need for task complexity when testing spatial memory in pigs. Housing conditions or individual behavioural style did not aVect spatial memory during MT1 or MT2. However, housing environment and behavioural style strongly aVected explorative behaviour of pigs in an unfamiliar maze during both exploration trials and memory tests. This implicates that apparent eVects of environmental enrichment on spatial learning and memory in pigs might reXect diVerences in explorative patterns rather than in cognitive processes.

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“…Such experiments were largely concerned with the consequences of dendritic growth in developing or adult rodents on memory encoding in relatively simple operant (rewarded) paradigms; the goal was not to assess the application of experience to current situations but rather to test if structural changes in brain are associated with improved performance (Kolb and Gibb 1991;Falkenberg et al 1992;Rosenzweig and Bennett 1996;Nilsson et al 1999;van Praag et al 2000;Leggio et al 2005). Our studies used much briefer, repeated exposures to enrichment that did not produce detectable changes in synapse numbers, and behavioral tests in very complex circumstances in which explicit rewards were absent.…”

Section: Discussionmentioning

confidence: 99%

“…Such networks could in principle be modified by either or both the strengthening of existing synapses, or the growth of dendrites and synaptogenesis (Maviel et al 2004;Restivo et al 2009; Lesburgueres et al 2011). Indeed, prolonged exposure to an enriched environment leads to the growth of dendritic branches and spines in hippocampus and cortex in rodents (Globus et al 1973;Greenough et al 1973;Lauterborn et al 2015) along with improved performance in a variety of rewarded learning tasks (Renner and Rosenzweig 1987;Kolb and Whishaw 1998;van Praag et al 2000;Kolb et al 2003;Leggio et al 2005). However, the immense capacity of memory presents difficulties for the latter hypothesis: experiential learning in complex circumstances is a routine event in humans and animals outside the laboratory and it seems likely that growth would quickly encounter limits.…”

Section: [Supplemental Materials Is Available For This Article]mentioning

confidence: 99%

Experiential learning in rodents: past experience enables rapid learning and localized encoding in hippocampus

et al. 2017

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Humans routinely use past experience with complexity to deal with novel, challenging circumstances. This fundamental aspect of real-world behavior has received surprisingly little attention in animal studies, and the underlying brain mechanisms are unknown. The present experiments tested for transfer from past experience in rats and then used quantitative imaging to localize synaptic modifications in hippocampus. Six daily exposures to an enriched environment (EE) caused a marked enhancement of short-and long-term memory encoded during a 30-min session in a different and complex environment relative to rats given extensive handling or access to running wheels. Relatedly, the EE animals investigated the novel environment in a different manner than the other groups, suggesting transfer of exploration strategies acquired in earlier interactions with complexity. This effect was not associated with changes in the number or size of excitatory synapses in hippocampus. Maps of synapses expressing a marker for long-term potentiation indicated that encoding in the EE group, relative to control animals, was concentrated in hippocampal field CA1. Importantly, <1% of the total population of synapses was involved in production of the regional map. These results constitute the first evidence that the transfer of experience profoundly affects the manner in which hippocampus encodes complex information. [Supplemental material is available for this article.]Transfer of learning is the capacity to effectively use abilities or information acquired in previous contexts in a new situation (Baldwin and Ford 1988;Perkins and Salomon 1992;Pan and Yang 2010). Importantly, learning and behavior in both the original and the new context may be self-directed, or may involve external guidance to varying degrees. Learning of the former typewithout external instruction, supervision, or reinforcement-is of particular interest and has been investigated in cognitive psychology (Fisher et al. 1991), education (Kolb 2015, perception and inference (Barlow 1989(Barlow , 1990, and machine learning (Hastie et al. 2009). It is widely recognized that the transfer of knowledge or strategies gained during learning to new situations is essential for the efficacy and flexibility of human behavior, particularly in unsupervised contexts. Despite this, there has been little work on whether and to what degree the effect occurs in laboratory animals. The present work used a combination of unsupervised experience with a complex environment followed by exposure to novel conditions to address this question. The results enabled a first investigation into how transfer affects the manner in which the hippocampus, a structure critical to unsupervised learning, encodes new information.We began with a straightforward extension of a well-known phenomenon: the reduction of spontaneous locomotor activity over time by rats in a novel open field. While open-field testing was originally introduced (Hall and Ballachey 1932) to measure emotionality, it became widely used as a simp...

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Environmental enrichment promotes improved spatial abilities and enhanced dendritic growth in the rat

Cited by 441 publications

References 79 publications

Environmental Enrichment Ameliorates Behavioral Impairments Modeling Schizophrenia in Mice Lacking Metabotropic Glutamate Receptor 5

Environmental Enrichment Ameliorates Behavioral Impairments Modeling Schizophrenia in Mice Lacking Metabotropic Glutamate Receptor 5

Spatial learning in pigs: effects of environmental enrichment and individual characteristics on behaviour and performance

Experiential learning in rodents: past experience enables rapid learning and localized encoding in hippocampus

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