White matter integrity correlates of implicit sequence learning in healthy aging

Abstract

Previous research has identified subcortical (caudate, putamen, hippocampus) and cortical (dorsolateral prefrontal cortex, DLPFC; frontal motor areas) regions involved in implicit sequence learning, with mixed findings for whether these neural substrates differ with aging. The present study used diffusion tensor imaging (DTI) tractography to reconstruct white matter connections between the known gray matter substrates, and integrity of these tracts was related to learning in the alternating serial reaction time task (ASRT) in younger and healthy older adults. Both age groups showed significant sequence learning (better performance to predictable, frequently occurring versus less frequent events), with an age-related difference in the late learning stage. Caudate-DLPFC and hippocampus-DLPFC tract integrity were related to ASRT sequence learning, and these brain-behavior relationships did not differ significantly between age groups. Additionally, age-related decreases in caudate-DLPFC tract integrity mediated age-related differences in late stage sequence learning. Together, these findings complement studies of gray matter substrates underlying implicit sequence learning, and provide evidence for similar white matter integrity-sequence learning relationships in younger and healthy older adults.

Caudate Resting Connectivity Predicts Implicit Probabilistic Sequence Learning

“…15), suggesting that our scan length is sufficient. Second, our sample size is relatively small, although comparable (or larger) than that of other published studies using similar tasks (e.g., Bennett et al, 2011;Rieckmann et al, 2010;Schendan et al, 2003;Simon et al, 2012). Since the chances of Type I error increase in small samples, however, replication with a larger sample is desirable, and future studies focusing on individual differences should consider acquiring longer scans.…”

“…This is not surprising in light of evidence indicating that a direct anatomical connection is not necessary for functional connectivity in the resting state (Honey et al, 2009). For SL, our earlier work using DTI tractography suggests that this DC-MTL functional relationship may be mediated via connections with the dorsolateral prefrontal cortex (DLPFC) (Bennett et al, 2011). Early in training, SL scores were positively correlated with the microstructural integrity of the tract between the right MTL and DLPFC, while later in training, learning scores positively correlated with the integrity of left caudate to DLPFC tract.…”

“…Evidence from studies using a variety of methods (including patient groups, diffusion tensor imaging [DTI], task-related functional magnetic resonance imaging [fMRI], and genetics) indicates that IPSL in the TLT and related SL tasks depends on the functional and structural integrity of a subcorticalcortical network, including the caudate, frontal cortices, and, potentially, the medial temporal lobes (MTL) (Bennett et al, 2011;Gheysen et al, 2011;Rieckmann et al, 2010;Rose et al, 2002;Schendan et al, 2003;Simon et al, 2011bSimon et al, , 2012Smith and McDowall, 2004;Wilkinson, et al, 2009). While frontal regions are thought to support the attentional and motorplanning demands of IPSL tasks, the caudate and, more controversially, the MTL may underlie the formation of associations that are necessary for learning in the tasks (Rose et al, 2002;Schendan et al, 2003;Simon et al, 2012).…”

Age-related prefrontal impairments implicate deficient prediction of future reward in older adults

“…On the one hand it could be argued that changes in prediction error signaling in OA are due to compromised dopamine (DA) projections to frontostriatal circuits (Dreher et al, 2008). On the other hand, there is also evidence for the idea that age-related changes in prediction error signals result from deficits in the connectivity between frontal and striatal regions in OA (Bennett et al, 2011;SamanezLarkin et al, 2012). Moreover, findings from multimodal imaging (positron emission tomography with fMRI) studies showed that striatal DA also affects frontal working memory and cognitive control functions (Braskie et al, 2008;Landau et al, 2009).…”

The key to success in elite athletes? Explicit and implicit motor learning in youth elite and non-elite soccer players

“…Moreover, a recent study showed that white matter integrity of the dentato-thalamo-cortical tract, connecting the lateral cerebellum to motor and prefrontal areas, is associated with motor sequence learning (Schulz Wessel, Zimerman, Timmermann, Gerloff, & Hummel, 2015). In addition, it has been shown that white matter integrity of these circuits predicts performance during implicit motor learning (Bennett, Madden, Vaidya, Howard, & Howard, 2011), which may lead to the suggestion that youth elite soccer players have better connectivity in these circuits. Our results are in line with studies on brain structure and functioning in experts on sports and music (Chang, 2014;Nakata et al, 2010;Roberts et al, 2012;Wei & Luo, 2010), supporting the relationship between general brain plasticity, motor learning skills and expertise.…”