Enrichment from Birth Accelerates the Functional and Cellular Development of a Motor Control Area in the Mouse

Abstract

BackgroundThere is strong evidence that sensory experience in early life has a profound influence on the development of sensory circuits. Very little is known, however, about the role of experience in the early development of striatal networks which regulate both motor and cognitive function. To address this, we have investigated the influence of early environmental enrichment on motor development.Methodology/Principal FindingsMice were raised in standard or enriched housing from birth. For animals assessed as adults, half of the mice had their rearing condition reversed at weaning to enable the examination of the effects of pre- versus post-weaning enrichment. We found that exclusively pre-weaning enrichment significantly improved performance on the Morris water maze compared to non-enriched mice. The effects of early enrichment on the emergence of motor programs were assessed by performing behavioural tests at postnatal day 10. Enriched mice traversed a significantly larger region of the test arena in an open-field test and had improved swimming ability compared to non-enriched cohorts. A potential cellular correlate of these changes was investigated using Wisteria-floribunda agglutinin (WFA) staining to mark chondroitin-sulfate proteoglycans (CSPGs). We found that the previously reported transition of CSPG staining from striosome-associated clouds to matrix-associated perineuronal nets (PNNs) is accelerated in enriched mice.Conclusions/SignificanceThis is the first demonstration that the early emergence of exploratory as well as coordinated movement is sensitive to experience. These behavioural changes are correlated with an acceleration of the emergence of striatal PNNs suggesting that they may consolidate the neural circuits underlying these behaviours. Finally, we confirm that pre-weaning experience can lead to life long changes in the learning ability of mice.

Effect of chronic stress during adolescence in prefrontal cortex structure and function

“…This pattern of PNN maturation had also been demonstrated in other developing cortical regions, such as the primary somatosensory cortex [38], the primary visual cortex [31,68] and subcortical regions including the amygdala [69] and the striatum [70]. This increase in PNN + neuron density is supposed to be associated with maturation of inhibitory circuits and to signal the closure of the critical period of plasticity of particular areas [71,72].…”

Development of motor maps in rats and their modulation by experience

“…In the enriched environment condition, the dam was removed from the large cage on PND 21 while all offspring remained. Enriched offspring had continuous enrichment, both before weaning and after weaning, for the duration of the experiment to ensure lifelong enrichment opportunities, as this has been shown to be an important variable (Simonetti et al 2009). In the deprived condition, offspring were separated from the dam and housed in pairs in standard shoebox cages and were not provided with any toys or additional items other than their standard food pellets, water bottle, and bedding.…”

The Use of the Puzzle Box as a Means of Assessing the Efficacy of Environmental Enrichment

“…Environmental enrichment (EE) may be defined as surroundings that provide animals with increased opportunity for social interaction, motor activity, and greater sensory stimulation than usually experienced in a standard laboratory environment.EE has been shown to consistently affect the behavior of animals, bringing about changes such as reduction of stress and anxiety-related activity [8][9][10] , improved performance in learning and memory tasks 8,11 , early onset of motor coordination and exploratory activity 11 , changes in maternal care 8 as well as resistance to addictive substances [12][13][14][15] . Further, EE has been revealed to ameliorate the effects of neurodegenerative disorders, delaying the onset and decreasing the severity of symptoms in animal models of Huntington's [1][2][3][4]16 , Parkinson's 17 and Alzheimer's disease 18 .…”