Nurturing brain plasticity: impact of environmental enrichment

Baroncelli, Laura; Braschi, Chiara; Spolidoro, Maria; Begenisic, Tatjana; Sale, Alessandro; Maffei, Lamberto

doi:10.1038/cdd.2009.193

Cited by 262 publications

(229 citation statements)

References 202 publications

(259 reference statements)

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“…The prominent role of reduced intracortical inhibition for promoting OD plasticity in EE mice does not rule out the involvement of additional mechanisms. It has been shown that, for example, neuromodulatory systems are affected by EE housing (35) and modulate OD plasticity (36-39). Brain-derived neurotrophic factor is increased after EE housing (18,19,40) and can reactivate OD plasticity (36).…”

Section: Discussionmentioning

confidence: 99%

Environmental enrichment extends ocular dominance plasticity into adulthood and protects from stroke-induced impairments of plasticity

Greifzu

Pielecka-Fortuna

Kalogeraki

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

130

208

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Ocular dominance (OD) plasticity in mouse primary visual cortex (V1) declines during postnatal development and is absent beyond postnatal day 110 if mice are raised in standard cages (SCs). An enriched environment (EE) promotes OD plasticity in adult rats. Here, we explored cellular mechanisms of EE in mouse V1 and the therapeutic potential of EE to prevent impairments of plasticity after a cortical stroke. Using in vivo optical imaging, we observed that monocular deprivation in adult EE mice (i) caused a very strong OD plasticity previously only observed in 4-wk-old animals, (ii) restored already lost OD plasticity in adult SC-raised mice, and (iii) preserved OD plasticity after a stroke in the primary somatosensory cortex. Using patch-clamp electrophysiology in vitro, we also show that (iv) local inhibition was significantly reduced in V1 slices of adult EE mice and (v) the GABA/AMPA ratio was like that in 4-wk-old SC-raised animals. These observations were corroborated by in vivo analyses showing that diazepam treatment significantly reduced the OD shift of EE mice after monocular deprivation. Taken together, EE extended the sensitive phase for OD plasticity into late adulthood, rejuvenated V1 after 4 mo of SCrearing, and protected adult mice from stroke-induced impairments of cortical plasticity. The EE effect was mediated most likely by preserving low juvenile levels of inhibition into adulthood, which potentially promoted adaptive changes in cortical circuits. O cular dominance (OD) plasticity induced by monocular deprivation (MD) is one of the best studied models of experience-dependent plasticity in the mammalian cortex (1, 2). OD plasticity in primary visual cortex (V1) of C57BL/6J mice is maximal at 4 wk of age, declines after 2-3 mo, and is absent beyond postnatal day 110 (PD110) if animals are raised in standard cages (SCs) (3-6). In 4-wk-old mice, 4 d of MD are sufficient to induce an OD shift to the open eye; therefore, neurons in the binocular V1, which are usually dominated by the contralateral eye in rodents (3, 7), become activated more equally by both eyes (5,8). This juvenile OD shift is predominantly mediated by a decrease in the visual cortical responses to the deprived eye (1, 9-11), whereas significant OD shifts in older animals up to PD110 need 7 d of MD and are mediated primarily by increased openeye responses in V1. Raising animals in an enriched environment (EE) gives them the opportunity of enhanced physical, social, and cognitive stimulation and influences brain physiology and behavior in many ways (12, 13). It has been shown previously that EE enhances visual system development in rats (14) and mice (15-17), increases levels of the brain-derived neurotrophic factor and serotonin (18), reduces both extracellular GABA levels (18, 19) and the density of ECM perineuronal nets (PNNs) (19), and promotes OD plasticity in adult and aging rats (18-21). Here, we explored cellular mechanisms of EE in V1 of mice and the therapeutic potential of EE to prevent impairments of plasticity after a c...

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Section: Discussionmentioning

confidence: 99%

Environmental enrichment extends ocular dominance plasticity into adulthood and protects from stroke-induced impairments of plasticity

Greifzu

Pielecka-Fortuna

Kalogeraki

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

130

208

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“…At the cellular level, these modifications underpin synaptic plasticity (Citri and Malenka, 2008;Ho et al, 2011), and in the whole animal support learning and memory (Morris, 2006;Neves et al, 2008) and its response to the environment (Nithianantharajah and Hannan, 2006;Baroncelli et al, 2010). These changes involve both functional and structural adaptations in terms of intrinsic excitability (Davis, 2006), postsynaptic glutamate receptor complement (Kerchner and Nicoll, 2008;Kessels and Malinow, 2009), neurotransmitter release (Citri and Malenka, 2008), and in the shape and density of dendritic spines, axonal arbors, and synaptic boutons (Holtmaat and Svoboda, 2009;Hübener and Bonhoeffer, 2010).…”

Section: Introductionmentioning

confidence: 99%

“…Increased BDNF mRNA and protein have been observed in rodents in response to environmental enrichment (Nithianantharajah and Hannan, 2006;Baroncelli et al, 2010), which, via the BDNF TrkB receptor, promotes dendritic growth and increased spine density in an ERK1/2-dependent manner (Cowansage et al, 2010). BDNF is also implicated in a form of synaptic adaptation known as homeostatic synaptic scaling in which suppression of neuronal firing in vitro by tetrodotoxin (TTX) causes a reduction in BDNF levels and a compensatory increase in synaptic strength, an observation that can be mimicked by BDNF TrkB receptor antagonists .…”

Section: Introductionmentioning

confidence: 99%

MSK1 Regulates Homeostatic and Experience-Dependent Synaptic Plasticity

Corrêa¹,

Hunter

Palygin³

et al. 2012

J. Neurosci.

128

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The ability of neurons to modulate synaptic strength underpins synaptic plasticity, learning and memory, and adaptation to sensory experience. Despite the importance of synaptic adaptation in directing, reinforcing, and revising the behavioral response to environmental influences, the cellular and molecular mechanisms underlying synaptic adaptation are far from clear. Brain-derived neurotrophic factor (BDNF) is a prime initiator of structural and functional synaptic adaptation. However, the signaling cascade activated by BDNF to initiate these adaptive changes has not been elucidated. We have previously shown that BDNF activates mitogen-and stress-activated kinase 1 (MSK1), which regulates gene transcription via the phosphorylation of both CREB and histone H3. Using mice with a kinase-dead knock-in mutation of MSK1, we now show that MSK1 is necessary for the upregulation of synaptic strength in response to environmental enrichment in vivo. Furthermore, neurons from MSK1 kinase-dead mice failed to show scaling of synaptic transmission in response to activity deprivation in vitro, a deficit that could be rescued by reintroduction of wild-type MSK1. We also show that MSK1 forms part of a BDNF-and MAPK-dependent signaling cascade required for homeostatic synaptic scaling, which likely resides in the ability of MSK1 to regulate cell surface GluA1 expression via the induction of Arc/Arg3.1. These results demonstrate that MSK1 is an integral part of a signaling pathway that underlies the adaptive response to synaptic and environmental experience. MSK1 may thus act as a key homeostat in the activity-and experience-dependent regulation of synaptic strength.

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“…Indeed, the visual cortex of enriched rats displays a remarkable reactivation of ocular dominance plasticity in response to MD [127,128]. The ocular dominance shift of cortical neurons is detectable using both VEPs and single-unit recordings.…”

Section: Serotonin: a Master Regulator Of Adult Neural Plasticitymentioning

confidence: 99%