Lifelong environmental enrichment in rats: impact on emotional behavior, spatial memory vividness, and cholinergic neurons over the lifespan

Abstract

We assessed lifelong environmental enrichment effects on possible age-related modifications in emotional behaviors, spatial memory acquisition, retrieval of recent and remote spatial memory, and cholinergic forebrain systems. At the age of 1 month, Long-Evans female rats were placed in standard or enriched rearing conditions and tested after 3 (young), 12 (middle-aged), or 24 (aged)months. Environmental enrichment decreased the reactivity to stressful situations regardless of age. In the water maze test, it delayed the onset of learning deficits and prevented age-dependent spatial learning and recent memory retrieval alterations. Remote memory retrieval, which was altered independently of age under standard rearing conditions, was rescued by enrichment in young and middle-aged, but unfortunately not aged rats. A protected basal forebrain cholinergic system, which could well be one out of several neuronal manifestations of lifelong environmental enrichment, might have contributed to the behavioral benefits of this enrichment.

Maternal exposure to environmental enrichment before and during gestation influences behaviour of rat offspring in a sex-specific manner

“…In our EE design, we hypothesize that 6-7 weeks of EE exposure to running wheel could have played a role in the female better cognitive performance. Our EE exposed females (future mothers) did not show modifications in anxiety-related behaviour in the EPM; literature studies show contrasting results in anxiety revealing tests (see introduction, [11][12][13][14][15][16][17]). …”

“…Much less investigated are the effects of EE on female rats. Only two studies show that enrichment in adulthood [14] or during pregnancy and lactation [49] does not induce significant changes of learning in the MWM. It is necessary to specify that in both studies, enrichment implied the inclusion of toys and various objects within the cage with the omission of a running wheel, thereby depriving animals of physical exercise.…”

Late enrichment maintains accurate recent and remote spatial memory only in aged rats that were unimpaired when middle aged

“…Only a few studies have assessed whether enrichment has an impact on remote memory. Enrichment was shown to enhance long-term memory for object recognition (i.e., 48 h after exposure) in both young (Bruel-Jungerman et al 2005;Leger et al 2015) and aged rats (Leal-Galicia et al 2008), and our team has previously shown that long-life environmental enrichment protects young and middle-aged rats against spontaneous forgetting (Harati et al 2013). The results of the present study extend these findings by showing that late enrichment also enables aged rats to form memory traces that are less sensitive to degradation.…”

“…Some of these studies also reported further decline following these ages (e.g., Bizon et al 2009;McQuail and Nicolle 2015). In Long-Evans female rats, previous cross-sectional studies by our team also showed impaired performance at 15 mo when compared with 6-mo-old subjects (Harati et al 2013), and further degradation of spatial reference memory between the age of 13-15 mo and 25-27 mo (Harati et al 2011(Harati et al , 2013. However, several studies highlighted the fact that the age-related decline in spatial memory reported in studies comparing age-groups concerns only some of the subjects (e.g., Gallagher et al 1993;McQuail and Nicolle 2015).…”

“…Several studies using cross-sectional experimental designs showed that spatial memory progressively declines during adulthood. Thus, performances of middle-aged subjects are impaired compared with those of younger adults, but less severely than those of elderly subjects (e.g., Wyss et al 2000;Bizon et al 2009;Harati et al 2013). Conversely, impaired spatial memory is not a systematic hallmark of physiological aging and many experiments have highlighted the heterogeneity of individual performance at a given chronological age (e.g., Gage et al 1984;Gallagher et al 1993;McQuail and Nicolle 2015).…”