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.
Probabilistic reinforcement learning declines in healthy cognitive aging. While some findings suggest impairments are especially conspicuous in learning from rewards, resembling deficits in Parkinson’s disease, others also show impairments in learning from punishments. To reconcile these findings, we tested 252 adults from three age groups on a probabilistic reinforcement learning task, analyzed trial-by-trial performance with a Q-reinforcement learning model, and correlated both fitted model parameters and behavior to polymorphisms in dopamine-related genes. Analyses revealed that learning from both positive and negative feedback declines with age, but through different mechanisms: When learning from negative feedback, older adults were slower due to noisy decision-making; when learning from positive feedback, they tended to settle for a non-optimal solution due to an imbalance in learning from positive and negative prediction errors. The imbalance was associated with polymorphisms in the DARPP-32 gene and appeared to arise from mechanisms different from those previously attributed to Parkinson’s disease. Moreover, this imbalance predicted previous findings on aging using the Probabilistic Selection Task, which were misattributed to Parkinsonian mechanisms.
Relating individual differences in cognitive abilities to neural substrates in older adults is of significant scientific and clinical interest, but remains a major challenge. Previous functional magnetic resonance imaging (fMRI) studies of cognitive aging have mainly focused on the amplitude of fMRI response, which does not measure neuronal selectivity and has led to some conflicting findings. Here, using local regional heterogeneity analysis, or Hcorr, a novel fMRI analysis technique developed to probe the sparseness of neuronal activations as an indirect measure of neuronal selectivity, we found that individual differences in two different cognitive functions, episodic memory and letter verbal fluency, are selectively related to Hcorr-estimated neuronal selectivity at their corresponding brain regions (hippocampus and visual-word form area, respectively). This suggests a direct relationship between cognitive function and neuronal selectivity at the corresponding brain regions in healthy older adults, which in turn suggests that age-related neural dedifferentiation might contribute to rather than compensate for cognitive decline in healthy older adults. Additionally, the capability to estimate neuronal selectivity across brain regions with a single data set and link them to cognitive performance suggests that, compared to fMRI-adaptation—the established fMRI technique to assess neuronal selectivity, Hcorr might be a better alternative in studying normal aging and neurodegenerative diseases, both of which are associated with widespread changes across the brain.
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