Introduction

Understanding the accompanying changes and the protective factors against cognitive aging has become a major health issue. Impaired episodic memory (involving retrieval of personal experiences and their spatial and temporal contexts) is one of the main concerns of older adults, and is well documented in the literature (see [1] for a meta-analysis). Episodic memory loss is greater in tasks that do not provide environmental support (e.g., free recall, [2,3,4]) and require participants to self-initiate efficient memory strategies. These tasks require more executive resources than those that provide environmental support (e.g., recognition).

Executive functions are defined as “a set of general-purpose control mechanisms, often linked to the prefrontal cortex of the brain, that regulate the dynamics of human cognition and action” [5]. These specific functions are involved in self-initiated memory strategies during encoding and retrieval (e.g., [6]). Several studies and meta-analyses have confirmed that executive functioning is impaired in aging, with a deficit in each specific function presented in Miyake et al.’s [7] model (i.e., inhibition, flexibility and updating; see [8] for a review). According to the executive hypothesis of aging [9], the age-related deficit in executive functions could explain episodic memory decline, especially in the most resource-demanding tasks, due to difficulty in self-initiating effective memory strategies [6, 10, 11].

Many individual differences in episodic memory performance can be observed among older adults, both qualitatively (e.g., vivacity and precision of recall) and quantitatively (e.g., number of correct recalls). These differences can be explained by cognitive reserve, defined as mechanisms that protect against cognitive decline [12]. Cognitive reserve allows older adults to compensate for decline through a more efficient use of cognitive processes. Thus, healthy older adults with high cognitive reserve show less episodic memory decline. Factors such as educational level, social and physical activities have been studied for their protective effects on episodic memory in advancing age [13].

Voelcker-Rehage et al. [14] showed that physical activity (PA) (grip force and spiroergometry, i.e., cardiovascular fitness) was positively related to performance on a modified version of the Flanker Task and N-Back task in older adults (see [39], we tested the significance of indirect effects using Preacher and Hayes’ [40] bootstrap** process for R version 4.1.1. Thus, when zero is included in the confidence interval, the effect cannot be considered as significant. By contrast, when zero is not included, the effect can be considered as significant.

Results

Results for the episodic memory task, executive functions and PA are presented in Table 2. No effect of age group on IAL and IAS [t(42) = 1.47; p = 0.149 and t(42) = -0.28; p = 0.781 respectively] or on the overall PA index [t(42) = 0.03; p = 0.975].

Table 2 Means (and SD) of memory scores, executive index and PA measures for each age group
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Episodic memory

The GLM conducted on episodic memory performance confirmed the age-group effect, F (1,40) = 90.85, p < 0.001, ηp2 = 0.69, with fewer words correctly recalled by older than younger adults. The results also showed an effect of PA, F (1,40) = 17.07, p < 0.001, ηp2 = 0.30. Correlational analyses indicated that PA was positively related to episodic memory performance (r = 0.32, p = 0.034). Finally, the interaction between age group and PA was significant, F (1,40) = 15.28, p < 0.001, ηp2 = 0.28. More precisely, to investigate this interaction, correlation analyses were conducted and indicated that the positive correlation between PA and memory performance was significant in older adults (r = 0.89, p < 0.001) but not in younger adults (r = -0.10, p = 0.695).

The GLM performed on the working-memory task revealed an effect of age group, F (1,40) = 35.43, p < 0.001, ηp2 = 0.47, with a higher percentage of errors by older than younger adults. This analysis also showed an effect of PA, F (1,40) = 10.14, p = 0.003, ηp2 = 0.20; participants with higher levels of PA made fewer errors on the working-memory task (r = -0.34, p = 0.024). This effect was similar in younger and older adults (respectively, r = -0.28, p = 0.244 and r = -0.57, p = 0.003), as there was no significant interaction between age and PA, F (1, 40) = 0.56, p = 0.458.

Executive index

The GLM performed on the executive index revealed an age-group effect, F (1,40) = 44.52, p < 0.001, ηp2 = 0.53, with better executive functioning in younger adults. The analysis also showed an effect of PA, F (1,40) = 15.88, p < 0.001, ηp2 = 0.28, with higher levels of PA corresponding to a higher executive index (r = 0.39, p = 0.010). Finally, a significant interaction was found between PA and executive index, F (1, 40) = 4.57, p = 0.039, ηp2 = 0.10, indicating that this relationship was significant only in older adults (r = 0.63, p = 0.001) and not in younger adults (r = 0.24, p = 0.315).

Regression analysis

Episodic memory performance and executive index were positively correlated (r = 0.60, p = 0.002) in older adults. Significant negative correlations were found between these two variables and the chronological age of older adults (r = -0.50, p = 0.01 for episodic memory, r = -0.67, p < 0.001 for executive index) and between PA and the chronological age of older adults (r = -0.56, p = 0.004 for PA). As these linear relationships were only found in older adults, regression analyses were performed only in this age group to better understand the underlying mechanisms of PA benefits on memory and executive functions in old age. The mediation model (including age, executive index and PA as predictors of memory performance) and the different pathways are presented in Fig. 2.

Fig. 2
figure 2

Mediation model and paths in older adults explaining episodic memory performance with age, PA and executive index as predictors. An arrow indicates that the effect of the first variable is mediated by the second variable (indicated by the arrowhead). Main findings: ABC indicates that the effect of age on memory could be predicted by executive functions. DEC indicates that the effect of age on memory could be predicted by PA. The significant indirect pathway (in black) indicates the effect of age on memory could be predicted by executive functions, which itself could be predicted by PA

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First, the regression analysis revealed a significant direct association between age and episodic memory performance (i.e., percentage of correctly recalled words), F (1,23) = 7.84, p = 0.010, explaining 25.4% of the variance. Age was negatively associated with memory performance (path C, b = -0.56; 95% CI [-0.88, -0.19]).

The simple mediation model predicting memory performance from age and executive index (paths A, B and C) was significant, F (2,22) = 6.70, p = 0.005, explaining 38% of the variance in memory performance. To go further, age was negatively associated with executive index (path A, b = -0.19; 95% CI [-0.29, -0.010]), and executive index was positively associated with memory performance (path B, b = 2.33; 95% CI [0.81, 3.34]). After controlling for executive functioning (b = 1.85; 95% CI [0.15, 3.12]), the negative association between age and memory performance was no longer significant (b = -0.20; 95% CI [-0.64, 0.20]). Importantly, the indirect effect explaining the effect of age on memory performance through executive index was significant, 95% CI [-0.76, -0.11].

The other simple mediation model predicting memory performance from age and PA (paths D, E and C) was also significant, F (2,22) = 40.37, p < 0.001, explaining 78% of the variance in memory performance. To go further, age was negatively associated with PA (path D, b = -0.23; 95% CI [-0.34, -0.11]) and PA was positively associated with memory performance (path E, b = 2.36; 95% CI [1.81, 2.76]). As in the previous model, after controlling for PA (b = 2.33; 95% CI [1.77, 2.85]), the negative association between age and memory performance was no longer significant (b = -0.02; 95% CI [-0.26, 0.24]). For this model, the indirect effect explaining the age effect on memory performance through PA was significant, 95% CI [-0.81, -0.31].

The overall mediation model predicting memory performance from age, executive index and PA was significant, F (3,21) = 26.23, p < 0.001, explaining 79% of the variance in memory performance. To go further, the executive index was positively associated with PA (path F, b = 0.91; 95% CI [0.52, 1.32]). Most importantly, the effects of age and executive index on memory performance were no longer significant (respectively, b = 0.03; 95% CI [-0.28, 0.34] and b = 0.34; 95% CI [-0.92, 1.35]) when PA (b = 2.25; 95% CI [1.68, 2.80]) was entered in the regression analysis. These important results show that the effects of both age and executive index on episodic memory are mediated by PA. In this mediation model, the indirect effects explaining the effect of age on memory performance through executive index (paths A and B) and through PA (paths D and E) were no longer significant, 95% CI [-0.28, 0.17] and 95% CI [-0.46, 0.07] respectively. The serial indirect pathway explaining the effect of age on memory performance through executive index and then PA (corresponding to paths A, F and E) was significant, 95% CI [-0.68, -0.06], suggesting that the effect of age on memory could be predicted by executive index, which itself could be predicted by PA.

As PA was also positively associated with executive index (reverse path F, b = 0.43; 95% CI [0.23, 0.64]), we tested the serial indirect pathway explaining the effect of age on memory performance through PA and then executive index (corresponding to paths D, reverse F and B). This indirect pathway was non-significant, 95% CI [-0.10, 0.05].

Discussion

Our main objective was to demonstrate that PA mediates both the effects of age and executive functions on the memory performance of older adults. Our results suggested that the benefits of PA on episodic memory can be explained by a lower executive decline. This is the first study to explore the effect of PA on an innovative episodic memory task that includes a high-load working memory task during the encoding phase, to highlight the importance of benefits on the strategic phases of memory recall. During encoding, the amount of executive resources available to encode the target words are reduced by a working-memory load. Theoretically, only participants with high executive resources could correctly encode the words presented. In addition, during the retrieval, participants specified an old/new judgment in order to identify episodic responses, for which the effects of PA seemed to emerge significantly.

Our results confirmed the effects of age on memory [1] and on the working-memory load [41]: younger adults correctly recalled more words and made fewer errors in the working-memory task than older adults. Interestingly, the results confirmed that PA could be beneficial for memory performance (e.g., [16, 19,20,21,22]), and showed that these benefits are not affected by a simultaneous resource-demanding task (i.e., working-memory task), which has not been demonstrated in previous studies. Moreover, the benefits of PA on episodic memory performance were only significant in older adults. Thus, engagement in PA maintains the episodic memory performance of older adults, in accordance with previous research (e.g., [16, 17]). The current study also confirmed the well-established effect of age (see [8] for a review) and the benefits of PA on executive functions, particularly for older adults [57,58,59]); further research is required to examine the effects of these changes on the benefits observed. Although there is a wealth of literature showing the benefits of PA on cognition, a better understanding of the underlying mechanisms is needed. Accordingly, as PA is one of several cognitive reserve factors, it would be interesting to replicate our results while controlling for others factor, as in Kachouri et al. [19], or examining a possible moderation effect of these other cognitive reserve factors on the effects of PA on memory. In this way, it would be possible to maximize the benefits of PA on cognitive performance by showing "how" these benefits exist and "who" benefits the most.