The effects of aging on the neural basis of implicit associative learning in a probabilistic triplets learning task

Abstract

Few studies have investigated how aging influences the neural basis of implicit associative learning, and available evidence is inconclusive. One emerging behavioral pattern is that age differences increase with practice, perhaps reflecting the involvement of different brain regions with training. Many studies report hippocampal involvement early on with learning becoming increasingly dependent on the caudate with practice. We tested the hypothesis that the contribution of these regions to learning changes with age because of differential age-related declines in the striatum and hippocampi. We assessed age-related differences in brain activation during implicit associative learning using the Triplets Learning Task. Over three event-related fMRI runs, 11 younger and 12 healthy older adults responded to only the third (target) stimulus in sequences of three stimuli ("triplets") by corresponding key press. Unbeknown to participants, the first stimulus' location predicted one target location for 80% of trials and another target location for 20% of trials. Both age groups learned associative regularities but differences in favor of the younger adults emerged with practice. The neural basis of learning (response to predictability) was examined by identifying regions that showed a greater response to triplets that occurred more frequently. Both age groups recruited the hippocampus early, but with training, the younger adults recruited their caudate whereas the older adults continued to rely on their hippocampus. This pattern enables older adults to maintain near-young levels of performance early in training, but not later, and adds to evidence that implicit associative learning is supported by different brain networks in younger and older adults.

Figure 1

Sample presentation of one triplet in Triplets Learning Task.

Figure 2

Difference of mean of median reaction times (RT) for Low – High Probability triplets in milliseconds over early, middle and late learning for younger (black) and older (white) adults in the fMRI study and younger adults in the separate behavioral study (cross-hatch). Error bars represent the standard error of the mean.

Figure 3

Clusters of activity in the left caudate in which younger adults show a greater response to predictability than older adults in early training. Graph shows contrast estimates, extracted from the mean of activated clusters using MARSBAR (±standard error) in younger and older adults (*p < 0.05).

Figure 4

Figure 4. Regions showing significant correlations between implicit associative learning scores and neural response to predictability in (A) younger adults and (B) older adults at late training, using a combined mask of the bilateral caudate and bilateral hippocampus (anatomically-defined). The scatter plot is presented to visualize how individual differences in the (C) caudate and (D) hippocampus relate to individual differences in late implicit associative learning within each age group. Contrast estimates were extracted from the mean of activated clusters using MARSBAR (Brett et al., 2002) in younger and older adults.