Memory quality modulates the effect of aging on memory consolidation during sleep: Reduced maintenance but intact gain

Abstract

Successful consolidation of associative memories relies on the coordinated interplay of slow oscillations and sleep spindles during non-rapid eye movement (NREM) sleep, enabling the transfer of labile information from the hippocampus to permanent memory stores in the neocortex. During senescence, the decline of the structural and functional integrity of the hippocampus and neocortical regions is paralleled by changes of the physiological events that stabilize and enhance associative memories during NREM sleep. However, the currently available evidence is inconclusive if and under which circumstances aging impacts memory consolidation. By tracing the encoding quality of single memories in individual participants, we demonstrate that previous learning determines the extent of age-related impairments in memory consolidation. Specifically, the detrimental effects of aging on memory maintenance were greatest for mnemonic contents of medium encoding quality, whereas memory gain of weakly encoded memories did not differ by age. Using multivariate techniques, we identified profiles of alterations in sleep physiology and brain structure characteristic for increasing age. Importantly, while both aged sleep and aged brain structure profiles were associated with reduced memory maintenance, inter-individual differences in neither sleep nor structural brain integrity qualified as the driving force behind age differences in sleep-dependent consolidation in the present study.