Novelty processing associated with neural beta oscillations improves recognition memory in young and older adults

Abstract

Novelty anticipation activates the mesolimbic system and promotes subsequent long-term memory in younger adults. Importantly, mesolimbic structures typically degenerate with age, which might reduce positive effects of novelty anticipation. Here, we used electroencephalography in combination with an established paradigm in healthy young (19-33 years old, n = 28) and older (53-84, n = 27) humans. Colored cues predicted the subsequent presentation of either a novel or previously familiarized image (75% cue validity). On the subsequent day, recognition memory for the novel images was tested. Behaviorally, novelty anticipation improved recollection-based but not familiarity-based recognition memory in both groups, and this effect was more pronounced in older subjects. Furthermore, novelty and familiarity cues increased theta (4-8 Hz) and decreased alpha/beta power (9-20 Hz); at outcome, expected novel and familiar images both increased beta power (13-25 Hz). Finally, a subsequent memory effect for expected novel images was associated with increases in beta power independent of age. Together, novelty anticipation drives hippocampus-dependent long-term recognition memory across the life span, and this effect appears to be related to neural beta oscillations.

Effects of exploring a novel environment on memory across the lifespan

“…A potential explanation for our findings is that novelty influenced motivation differently across age groups (as suggested by the NOvelty-related Motivation of Anticipation and exploration by Dopamine model [NOMAD] 32 . The mesolimbic dopamine system is strongly associated with motivation 57 , 58 , but this system also has been suggested to underlie the effects of novelty on memory 59 , 60 . As such, the effects of novelty through dopaminergic modulation as described above, would likely share neural pathways with potential effects of novelty on motivation.…”

Differential effects of expectancy on memory formation in young and older adults

“…Anticipating novel information differs from other domains, such as rewards or known visual information, since it is more abstract and as such more difficult to envision. Therefore, it is not surprising that the effects of novelty on learning and the underlying neural processes also appear to differ, as suggested by recent studies using electroencephalography (EEG) (Schomaker & Meeter, 2018; Steiger et al, 2022). More specifically, neural activity and memory performance was associated with novelty prediction, but not the prediction error (Steiger et al, 2022), which can be defined as difference between expected and received information.…”

“…Therefore, it is not surprising that the effects of novelty on learning and the underlying neural processes also appear to differ, as suggested by recent studies using electroencephalography (EEG) (Schomaker & Meeter, 2018; Steiger et al, 2022). More specifically, neural activity and memory performance was associated with novelty prediction, but not the prediction error (Steiger et al, 2022), which can be defined as difference between expected and received information. Importantly, while some studies, including our own work (Steiger et al, 2022; Wittmann et al, 2007), provide evidence that anticipating a novel stimulus enhances memory for this information, others did not (Kafkas, 2021; Reichardt et al, 2022).…”

“…The processing of novel information has several benefits on cognition. It improves goal‐directed behavior (Düzel et al, 2010), enhances attention (Sokolov, 1963) and memory encoding (Cen et al, 2021; Schomaker, 2019; Steiger et al, 2022). Importantly, the underlying brain structures, including substantia nigra/ventral tegmental area (SN/VTA) and medial temporal lobe (MTL), are known to degenerate during healthy aging (Backman et al, 2006; Bunzeck et al, 2007; Fearnley & Lees, 1991) often with negative consequences on learning and memory (Schomaker et al, 2022).…”

“…More specifically, neural activity and memory performance was associated with novelty prediction, but not the prediction error (Steiger et al, 2022), which can be defined as difference between expected and received information. Importantly, while some studies, including our own work (Steiger et al, 2022; Wittmann et al, 2007), provide evidence that anticipating a novel stimulus enhances memory for this information, others did not (Kafkas, 2021; Reichardt et al, 2022). While this can have experimental reasons, it has also been suggested that different types of novelty (Schomaker & Meeter, 2015) and prior expectations play an important role (Quent et al, 2021).…”