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

Greifzu, Franziska; Pielecka-Fortuna, Justyna; Kalogeraki, Evgenia; Krempler, Katja; Favaro, Plinio D.; Schlüter, Oliver M.; Löwel, Siegrid

doi:10.1073/pnas.1313385111

Cited by 133 publications

(243 citation statements)

References 53 publications

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“…We showed that environmental enrichment can prolong and reinstate juvenilelike ODP, whereas the measured AMPA/NMDA receptor ratio was unchanged in V1 of adult enriched mice, and thus it is unlikely that generation of new silent synapses was induced (69). Thus, either different expression mechanisms could cause the same system level read-out with depression of deprived eye responses or the expression mechanism is independent of the existence of silent synapses.…”

Section: Discussionmentioning

confidence: 83%

“…Standard whole-cell voltage-clamp recordings and minimal stimulation procedures from coronal V1 slices were carried out using standard procedures as previously described (23,24,69). For AMPA/NMDA receptor ratios, the AMPA receptor component was measured as a peak value at V h = −60 mV and the NMDA receptor component was measured at V h = +40 mV at 60 ms after the AMPA receptor peak.…”

Section: Methodsmentioning

confidence: 99%

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Progressive maturation of silent synapses governs the duration of a critical period

Huang

Stodieck

Goetze

et al. 2015

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

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172

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During critical periods, all cortical neural circuits are refined to optimize their functional properties. The prevailing notion is that the balance between excitation and inhibition determines the onset and closure of critical periods. In contrast, we show that maturation of silent glutamatergic synapses onto principal neurons was sufficient to govern the duration of the critical period for ocular dominance plasticity in the visual cortex of mice. Specifically, postsynaptic density protein-95 (PSD-95) was absolutely required for experience-dependent maturation of silent synapses, and its absence before the onset of critical periods resulted in lifelong juvenile ocular dominance plasticity. Loss of PSD-95 in the visual cortex after the closure of the critical period reinstated silent synapses, resulting in reopening of juvenile-like ocular dominance plasticity. Additionally, silent synapse-based ocular dominance plasticity was largely independent of the inhibitory tone, whose developmental maturation was independent of PSD-95. Moreover, glutamatergic synaptic transmission onto parvalbumin-positive interneurons was unaltered in PSD-95 KO mice. These findings reveal not only that PSD-95-dependent silent synapse maturation in visual cortical principal neurons terminates the critical period for ocular dominance plasticity but also indicate that, in general, once silent synapses are consolidated in any neural circuit, initial experience-dependent functional optimization and critical periods end.

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Section: Discussionmentioning

confidence: 83%

Section: Methodsmentioning

confidence: 99%

Progressive maturation of silent synapses governs the duration of a critical period

Huang

Stodieck

Goetze

et al. 2015

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

Self Cite

172

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“…Mice show many of the expected responses to temporary MD, including robust depression of deprived-eye responses. However, one unusual feature of mouse ocular dominance plasticity is that it persists well into adulthood (42), particularly when visual experience is enriched (49,50). An additional complication is that the ocular dominance shift initiated in adults reverts spontaneously when binocular vision is restored (51,52) or if both eyelids are closed (53).…”

Section: Discussionmentioning

confidence: 99%

Rapid recovery from the effects of early monocular deprivation is enabled by temporary inactivation of the retinas

Fong

Mitchell

Duffy

et al. 2016

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

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A half-century of research on the consequences of monocular deprivation (MD) in animals has revealed a great deal about the pathophysiology of amblyopia. MD initiates synaptic changes in the visual cortex that reduce acuity and binocular vision by causing neurons to lose responsiveness to the deprived eye. However, much less is known about how deprivation-induced synaptic modifications can be reversed to restore normal visual function. One theoretically motivated hypothesis is that a period of inactivity can reduce the threshold for synaptic potentiation such that subsequent visual experience promotes synaptic strengthening and increased responsiveness in the visual cortex. Here we have reduced this idea to practice in two species. In young mice, we show that the otherwise stable loss of cortical responsiveness caused by MD is reversed when binocular visual experience follows temporary anesthetic inactivation of the retinas. In 3-mo-old kittens, we show that a severe impairment of visual acuity is also fully reversed by binocular experience following treatment and, further, that prolonged retinal inactivation alone can erase anatomical consequences of MD. We conclude that temporary retinal inactivation represents a highly efficacious means to promote recovery of function. A mblyopia is a widespread form of human visual disability that arises from imbalanced visual experience in the two eyes during infancy or early childhood. The core pathophysiological process underlying amblyopia is ocular dominance plasticity in the primary visual cortex (V1). Ocular dominance plasticity, evolutionarily conserved in mammals with binocular vision, has become a classic paradigm for studying how brain development is influenced by experience and deprivation. A brief period of monocular deprivation (MD) during early postnatal life causes functional depression of synapses in V1 that serve the deprived eye (1-7). Consequently, early-life MD severely and persistently degrades visual acuity through the deprived eye, which typically fails to recover spontaneously when binocular vision is restored (8-10). A critical step in developing targeted interventions for treating amblyopia is to identify strategies for reversing deprivation-driven synaptic modifications in V1.The traditional approach to promote recovery following MD has been to occlude the strong eye to force vision through the weak amblyopic eye. This "reverse occlusion" approach has been validated in animals (11, 12) and represents the cornerstone of current treatment (patching therapy) of human amblyopia (13-16). However, this treatment has well-known limitations that include poor compliance, potential loss of vision through the newly patched eye, failure to recover binocular vision, and a declining treatment efficacy with age (15, 17-21). Nevertheless, the success of reverse occlusion strategies demonstrates that severely weakened synaptic inputs in the brain can be rejuvenated under appropriate circumstances.An insight into how reverse occlusion might promote recovery came fr...

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“…To better understand the molecular factors by which EE exerts its impact on visual cortex plasticity, we studied histone acetylation at the promoters of the gene encoding BDNF, a factor crucially involved in developmental plasticity in the primary visual cortex and in the effects of early exposure to EE (Huang et al, 1999;.…”

Section: Histone Acetylation At the Bdnf Gene Promotermentioning

confidence: 99%

Experience Affects Critical Period Plasticity in the Visual Cortex through an Epigenetic Regulation of Histone Post-Translational Modifications

et al. 2016

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During an early phase of enhanced sensitivity called the critical period (CP), monocular deprivation causes a shift in the response of visual cortex binocular neurons in favor of the nondeprived eye, a process named ocular dominance (OD) plasticity. While the time course of the CP for OD plasticity can be modulated by genetic/pharmacological interventions targeting GABAergic inhibition, whether an increased sensory-motor experience can affect this major plastic phenomenon is not known. We report that exposure to environmental enrichment (EE) accelerated the closure of the CP for OD plasticity in the rat visual cortex. Histone H3 acetylation was developmentally regulated in primary visual cortex, with enhanced levels being detectable early in enriched pups, and chromatin immunoprecipitation revealed an increase at the level of the BDNF P3 promoter. Administration of the histone deacetylase inhibitor SAHA (suberoylanilide hydroxamic acid) to animals reared in a standard cage mimicked the increase in H3 acetylation observed in the visual cortex and resulted in an accelerated decay of OD plasticity. Finally, exposure to EE in adulthood upregulated H3 acetylation and was paralleled by a reopening of the CP. These findings demonstrate a critical involvement of the epigenetic machinery as a mediator of visual cortex developmental plasticity and of the impact of EE on OD plasticity.

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

Cited by 133 publications

References 53 publications

Progressive maturation of silent synapses governs the duration of a critical period

Progressive maturation of silent synapses governs the duration of a critical period

Rapid recovery from the effects of early monocular deprivation is enabled by temporary inactivation of the retinas

Experience Affects Critical Period Plasticity in the Visual Cortex through an Epigenetic Regulation of Histone Post-Translational Modifications

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