Environmental enrichment is associated with favorable memory-related functional brain activity patterns in older adults

Abstract

Background: In humans, environmental enrichment (EE), as measured by the engagement in a variety of leisure activities, has been associated with larger hippocampal structure and better memory function. The present cross-sectional study assessed whether EE during early life (13-30 years) and midlife (30-65 years) is associated with better preserved memory-related brain activity patterns in older age.

Methods: In total, 372 cognitively unimpaired older adults (aged ≥60 years old) of the DZNE-Longitudinal Study on Cognitive Impairment and Dementia (DELCODE; DRKS00007966) were investigated. EE was operationalized using items of the Lifetime of Experiences Questionnaire (LEQ), which measures the self-reported participation in a variety of leisure activities in early life and midlife. The preservation of memory-related functional brain activity was assessed using single-value scores, which relate older adults' brain activity patterns in the temporo-parieto-occipital memory network to those of young adults during visual memory encoding (FADE and SAME scores).

Results: EE during early life and midlife was significantly associated with higher SAME scores during novelty processing (n = 372, β = 0.13, p = 0.011). Thus, older participants with higher EE showed greater similarity of functional brain activity patterns during novelty processing with young adults. This positive association was observed most strongly in participants with subjective cognitive decline (SCD, n = 199, β = 0.20, p = 0.006).

Conclusion: More frequent participation in a variety of leisure activities in early life and midlife is associated with more successful aging of functional brain activity patterns in the memory network of older adults, including participants at increased risk for dementia. Longitudinal studies are needed to clarify whether higher EE during life could help preserve memory network function in later life.

Keywords: dementia; memory network; multimodal leisure activities; prevention; subjective cognitive decline.

Figure 1

Process of participant selection. The initial sample size of the DELCODE baseline dataset (data release for this study: 01.2021) was N = 1,079. Out of these, n = 468 had complete MRI data and thus FADE-SAME scores available. After exclusion of two participants with missing baseline LEQ and demographic data and 94 participants with a diagnosis of AD or MCI, the final sample amounted to n = 372 participants with 197 women and 175 men and the following subgroups: n = 127 OA, n = 199 participants with SCD, and n = 46 participants with FH. FADE/SAME, functional activity deviation during encoding/similarity of activations during memory encoding; LEQ, Lifetime of Experiences Questionnaire; AD, Alzheimer’s Dementia; MCI, mild cognitive impairment; OA, cognitively unimpaired older adults; SCD, subjective cognitive decline; FH, family history of AD.

Figure 2

Comprehensive overview of the FADE-SAME scores. ¹FADE scores reflect the deviation of functional brain activity during novelty processing and memory encoding. ²SAME scores reflect the similarity of activations (and deactivations) during novelty processing and memory encoding. FADE and SAME scores are inversely correlated, since the FADE score captures the deviation of functional activity patterns, whereas the SAME score captures the similarity of functional activity patterns. However, the SAME score also quantifies reduced deactivations, most prominently in default mode network (DMN) regions. Thus, FADE and SAME scores are rather complementary measures of successful aging in memory seen with respect to young adults (Soch et al., 2021; Richter et al., 2023). FADE, functional activity deviation during encoding; SAME, similarity of activations during memory encoding.

Figure 3

Association between environmental enrichment and SAME scores from the novelty contrast. Scatter plots display the unadjusted association between environmental enrichment and SAME scores from the novelty contrast (A) in the entire sample and (B) in the three subgroups. Environmental enrichment was significantly associated with SAME scores from the novelty contrast in the entire sample (p = 0.011) and in participants with subjective cognitive decline (p = 0.006). Since the FIML method merely estimates regression parameters, but not the missing values themselves, the 342 complete cases constitute the scattered data points; the parameters of the regression line itself (i.e., intercept and slope) are derived from the linear regression with FIML. *p < 0.05. β, standardized coefficient; SAME, similarity of activations during memory encoding.