Implicit associative learning relates to basal ganglia gray matter microstructure in young and older adults

Abstract

Older adults are impaired at implicit associative learning (IAL), or the learning of relationships between stimuli in the environment without conscious awareness. These age effects have been attributed to differential engagement of the basal ganglia (e.g. caudate, globus pallidus) and hippocampus throughout learning. However, no studies have examined gray matter diffusion relations with IAL, which can reveal microstructural properties that vary with age and contribute to learning. In this study, young (18-29 years) and older (65-87 years) adults completed the Triplet Learning Task, in which participants implicitly learn that the location of cues predict the target location on some trials (high frequency triplets). Diffusion imaging was also acquired and multicompartment diffusion metrics were calculated using neurite orientation dispersion and density imaging (NODDI). As expected, results revealed age deficits in IAL (smaller differences in performance to high versus low frequency triplets in the late learning stage) and age-related differences in basal ganglia and hippocampus free, hindered, and restricted diffusion. Significant correlations were seen between restricted caudate diffusion and early IAL and between hindered globus pallidus diffusion and late IAL, which were not moderated by age group. These findings indicate that individual differences in basal ganglia, but not hippocampal, gray matter microstructure contribute to learning, independent of age, further supporting basal ganglia involvement in IAL.

Age group differences in learning-related activity reflect task stage, not learning stage

“…Behaviorally, we observed age group differences in IAL as significantly faster reaction times to HF than LF triplets with this difference being larger during late versus early stages of learning and in younger versus older adults (Franco et al, 2020). Of note, no participant was able to accurately identify relationships between the cues and targets, supporting the notion that the associations were learned without awareness and were not the result of different explicit learning strategies between younger and older adults.…”

“…Participants completed eight runs of a modified version of the TLT (Howard et al, 2008;Simon et al, 2012), as previously reported (Franco et al, 2020). In this IAL task, participants viewed four open circles presented in a row on a white background.…”

“…Mean accuracy and mean of median reaction times were calculated for each block and each triplet type (HF, LF), and then averaged within each run. Mean of median reaction times were logarithmically transformed to control for age-related slowing (Franco et al, 2020;Simon et al, 2010). We then calculated learning scores for each participant as the difference in mean of median reaction times between the triplet types (LF -HF) across the first three (early) or last three (late) runs, such that positive values were indicative of better learning (i.e., a larger trial type difference).…”

“…As previously reported (Franco et al, 2020), age-related differences in IAL were assessed using separate Age Group (younger, older) x Triplet Type (HF, LF) x Learning Stage (early, late) mixed-design analysis of variance (ANOVAs) for each behavioral metric (log transformed mean of median reaction time, mean accuracy). For reaction time (Figure 1), evidence of IAL was seen as a significant main effect of Triplet Type, F(1, 48) = 43.08, p < 0.001, and a Triplet Type by Learning Stage interaction, F(1, 48) = 9.24, p < 0.001, indicating that participants were faster to HF (2.687 ± 0.063 msec) than LF (2.704 ± 0.057 msec) triplets and that the difference between HF and LF triplets was larger during late (difference: 0.019 ± 0.017 msec) than early (difference: 0.008 ± 0.022 msec) learning.…”

“…To better understand the neural substrates of age-related associative learning deficits, we acquired fMRI data from 28 younger and 22 older healthy adults who previously demonstrated significant age group differences in IAL (Franco et al, 2020). Here, we aimed to assess age group differences in (1) IAL-related activity in the hippocampus, basal ganglia, and prefrontal cortex, (2) relationships between IAL performance and IAL-related activity in these regions, and…”