Aged rats with different performances at environmental enrichment onset display different modulation of habituation and aversive memory

A wide agreement exists that environmental enrichment (EE) is most beneficial if introduced early in life, but numerous studies reported that also aged animals remain responsive. As age-related memory and cognition impairments are not uniform, an open question is whether EE might exert different effects in animals with different age-related deficits. A 12-week EE protocol was applied to late adult rats pretested for habituation and aversive memory. Animals were classified as low (LP) and high (HP) performers according to percent exploration change in Open Field test (OF) and as impaired (I) and not impaired (NI) according to latency in Step-through Passive Avoidance test (PA). Standard housing (SH) animals pretested by OF and PA, and naïve (non-pretested) EE and SH rats were used as controls. In comparison to pretest, after the housing protocol, EE LP ameliorated while EE HP and both SH HP and LP worsened their habituation pattern. The positive influence of EE on LP was probably due to the more active interaction with and the faster adaptation to surroundings promoted by continuous, multiple stimuli provided during the enriched housing. Regarding HP, EE did not boost the basal behavior, which likely represented the maximum achievable for that age, and the post housing exploration change dropped, as in SH animals, because of the retesting. After EE, a significant percentage of NI animals became I and a significant percentage of I animals became NI. The changes evidenced in the NI group likely depended on EE-related reduction of anxiety and the consequent more efficient coping with fearful situations. This hypothesis was strengthened by the observation that naïve EE animals were almost all I. Pretested EE I rats were not influenced by the rearing condition: their behavior was comparable to SH animals’ behavior and determined by retesting. In conclusion, these results demonstrated that, when applied to aging rats, EE produces different effects based on pre-housing cognitive performances. The issue needs further analyses, but the observation that not all animals are able to take advantage of EE to the same extent suggests the opportunity to design individually tailored approaches to optimize their efficacy and minimize possible unwanted consequences.