Short report
A rich environmental experience reactivates visual cortex plasticity in aged rats

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Abstract

Brain aging is characterized by functional deterioration across multiple systems, associated to a progressive decay of neural plasticity. Here, we explored environmental enrichment (EE), a condition of enhanced sensory-motor and cognitive stimulation, as a strategy to restore plasticity processes in the old brain. Visual system is one of the paradigmatic models for studying experience-dependent plasticity. While reducing input from one eye through monocular deprivation induces a marked ocular dominance (OD) shift of neurons in the primary visual cortex during development, the same manipulation is totally ineffective after the closure of the critical period. We show that EE is able to reactivate OD plasticity in the visual cortex of aging rats, as assessed with both visual-evoked potentials and single-unit recordings. A marked reduction in intracortical GABAergic inhibition and a remodeling of extracellular matrix accompany this effect. The non-invasive nature of EE makes this paradigm eligible for human application.

Highlights

► Environmental enrichment (EE) reactivates plasticity in the aged visual cortex. ► EE leads to decreased intracortical inhibition and extracellular matrix remodeling. ► Our results encourage the application of protocols based on EE to aging people.

Introduction

In the past few decades, decreased birth rate and longer life expectancy due to improved environmental conditions and medical assistance caused a marked world population aging and the emergence of age-related diseases as major determinants of human mortality. Complementary to efforts aimed at the characterization of pathological aging, defining cellular and molecular mechanisms underlying normal aging and finding tools capable to prevent or reverse age-related decline in the organism function are primary goals of both basic and clinical research in Neuroscience (Bishop et al., 2010).

The brain aging process is typically associated with functional deterioration across multiple systems, including cognitive and sensory-motor domains, that can, in part, be explained by a progressive decay of neural plasticity, i.e., the capacity to reorganize cerebral circuits in response to instructive and adaptive signals from the surrounding environment (Burke and Barnes, 2006). Despite the increasing evidence that environmental enrichment (EE) attenuates age-related cognitive deficits (Frick and Benoit, 2010), little is known about the effects of enhanced environmental stimulation on experience-dependent plasticity processes in the cerebral cortex of aging animals. The visual system stands as the prime model for studying neuronal plasticity. Occluding one eye early in development (monocular deprivation, MD) leads to an ocular dominance (OD) shift of cortical neurons, that is, a reduction in the number of cortical cells responding to that eye and a robust increment in the number of neurons activated by the open eye. The same treatment is completely ineffective in the adult organism (Berardi et al., 2000).

Recently, we challenged this dogma, demonstrating that EE in adult animals reactivates juvenile-like OD plasticity in the visual cortex (Baroncelli et al., 2010). In the effort to start studying whether exposure to enhanced stimulating conditions might favor experience-dependent plasticity in aged rats, we used in vivo electrophysiological recordings to measure OD plasticity in the visual cortex of monocularly-deprived aged rats exposed to either EE or normal standard rearing conditions. We provide evidence that aged rats are still sensitive to the reinstatement of plasticity induced by EE.

Section snippets

Animal treatment

A total of 27 female Long–Evans hooded rats (350–400 g) were used in this study, approved by the Italian Ministry of Public Health. At 22–23 months of age the animals were transferred for three weeks to an environmental enrichment (EE) setting or maintained in standard conditions (SC). Environmental enrichment consisted of a large cage (100 × 50 × 82 cm) with three floors linked by stairs, containing several food hoppers, free-access running wheels (diameter 25 cm) and differently shaped objects, which

Results

We evaluated OD plasticity in aged rats (22–23 months) housed either in environmental enrichment (EE) or in standard conditions (SC). Detrimental effects of aging, indeed, are self-evident in rats only after 20 months of age, with broadly expressed signs of deterioration in the limbic and sensory-motor systems not recognizable in younger adult animals (Frick and Benoit, 2010). After 7 days of MD, we recorded visual evoked potentials (VEPs) from Oc1B contralateral to the occluded eye, calculating

Discussion

We have demonstrated that an enhanced environmental stimulation is able to restore OD plasticity in the aging visual cortex. To make sure that plasticity was not present only at the level of subthreshold modifications of postsynaptic potentials (detected by VEPs), we measured OD properties of cortical neurons also using single-cell recordings. We reported a significant OD shift in the visual cortex contralateral to the deprived eye in MD–EE animals, though slightly lower with respect to that

Disclosure statement

The authors have read the disclosure of potential conflicts of interest and have nothing to declare.

Acknowledgements

The research was supported by the “Train the brain” grant from Fondazione Cassa di Risparmio di Pisa to Lamberto Maffei.

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These authors equally contributed to this work.

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