Neurophysiological markers of successful learning in healthy aging

Abstract

The capacity to learn and memorize is a key determinant for the quality of life but is known to decline to varying degrees with age. However, neural correlates of memory formation and the critical features that determine the extent to which aging affects learning are still not well understood. By employing a visual sequence learning task, we were able to track the behavioral and neurophysiological markers of gradual learning over several repetitions, which is not possible in traditional approaches that utilize a remember vs. forgotten comparison. On a neurophysiological level, we focused on two learning-related centro-parietal event-related potential (ERP) components: the expectancy-driven P300 and memory-related broader positivity (BP). Our results revealed that although both age groups showed significant learning progress, young individuals learned faster and remembered more stimuli than older participants. Successful learning was directly linked to a decrease of P300 and BP amplitudes. However, young participants showed larger P300 amplitudes with a sharper decrease during the learning, even after correcting for an observed age-related longer P300 latency and increased P300 peak variability. Additionally, the P300 amplitude predicted learning success in both age groups and showed good test–retest reliability. On the other hand, the memory formation processes, reflected by the BP amplitude, revealed a similar level of engagement in both age groups. However, this engagement did not translate into the same learning progress in the older participants. We suggest that the slower and more variable timing of the stimulus identification process reflected in the P300 means that despite the older participants engaging the memory formation process, there is less time for it to translate the categorical stimulus location information into a solidified memory trace. The results highlight the important role of the P300 and BP as a neurophysiological marker of learning and may enable the development of preventive measures for cognitive decline.

Pre-stimulus Activity Mediates Event-Related Theta Synchronization and Alpha Desynchronization During Memory Formation in Healthy Aging

“…Van der Linden, Brédart, and Beerten (1994) suggest that attentional resources linked to the frontal cortex undergo a marked decline with aging whereas the storage capacity remains relatively unaffected 65 . Previously, we demonstrated that the slower and more variable timing of the stimulus identification process, reflected in the event-related potential P300 latency, suggests that despite the older participants engaging the memory formation process to a comparable extent as young participants, there is less time for it to translate the stimulus location information into a solidified memory trace 37 . This aligns with the cognitive slowing theory, suggesting that slower processing in older participants leads to reduced working memory capacity.…”

“…The data used in this study was recorded in our laboratory in the context of a larger project that aims to quantify age effects on eye movement behavior and electroencephalography (EEG) recordings of resting-state and other task-based paradigms 37,38 . The data was collected in two experimental sessions separated by a week.…”

“…A visual sequence learning paradigm was first developed by Moisello et al (2013) and is currently considered as an important tool in assessing reliable indices of memory formation and learning progress 37,41 . Through the employment of simplified stimuli, this paradigm has the advantage of mitigating confounding effects of stimuli properties such as memorability, semantic content, and sensory characteristics that typically influence learning efficacy.…”

“…To provide stronger evidence for the link between mid-frontal theta ERS, parietal alpha ERD, and learning processes, we examined if the modulations of these components change as a function of learning state, that is, from stimulus being unknown, to newly learned, known and finally very well known (Supplementary Material 5. 4), independent of sequence repetition 37,41 . To further substantiate the connection between mid-frontal theta ERS and the process of learning, as well as parietal alpha ERD and learning, we aligned the sequence repetitions to the point where the sequence was correctly recalled for the first time (i.e., considering the number of repetitions before or after this point).…”