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

Abstract

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.

Neglect as a Violation of Species-Expectant Experience: Neurodevelopmental Consequences

“…(83) Other mechanisms are also involved, including changes in epigenetic regulation,(84) although we do not review those mechanisms here.…”

Environmental Enrichment Rescues Visually-Mediated Behavior in Ten-m3 Knockout Mice During an Early Critical Period

“…EE may also induce changes at other levels of the visual pathway, including the retina (Landi et al, 2007) and V1 (Ciucci et al, 2007;Sale et al, 2007;Levine et al, 2017), which may contribute to the behavioral recovery. In V1, exposure to EE has been shown to accelerate, in juvenile rodents (Cancedda et al, 2004;Baroncelli et al, 2016), as well as re-activate, in adult (Sale et al, 2007;Baroncelli et al, 2010) and even-aged rodents (Scali et al, 2012;Greifzu et al, 2016), the capacity for ocular dominance plasticity. EE may be exerting a similar effect in V1 in our mice which could be contributing to the observed recovery improvement in flight responses.…”

“…In the visual cortex, EE has been shown to extend the usual juvenile period of cortical plasticity which enables recovery from amblyopia into adulthood (Sale et al, 2007;Baroncelli et al, 2010Baroncelli et al, , 2016Scali et al, 2012;Greifzu et al, 2016), as well as accelerating the maturation of neural circuits in young mice (Cancedda et al, 2004;Ciucci et al, 2007). Benefits of EE on hippocampal function have also been demonstrated (Bernstein, 1973;van Praag et al, 2000;Speisman et al, 2013).…”

Activity-Dependent Remodeling ofDrosophilaOlfactory Sensory Neuron Brain Innervation during an Early-Life Critical Period

“…Typically, critical periods open with the onset of sensory experience and close after a defined period of refinement, during which neural circuitry is modified to better respond to the sensory environment (Hensch, 2005). Although initial studies painted a stark black-and-white picture regarding opening and closing of critical periods, it is now known that numerous factors can reopen critical period-like states in mature animals (McGee et al, 2005;Maya Vetencourt et al, 2008;Morishita et al, 2010;Hensch and Bilimoria, 2012;Baroncelli et al, 2016). Critical period work has focused primarily on vertebrate systems, but there are excellent examples of critical periods in invertebrate models (Fielde, 1904;Remy and Hobert, 2005;Doll and Broadie, 2015;Jin et al, 2016).…”