Modulation of fronto-parietal and autonomic activity underpins preserved working memory in middle-aged adults
Cognitive aging is a heterogeneous process, often diverging from chronological age. However, it remains unclear when early signs of cognitive decline emerge and which neurophysiological markers distinguish age-related cognitive alteration from preserved performances. This study aimed to identify early indicators of cognitive versus chronological aging. In a group of middle-aged adults (MA, n = 60), we distinguished high performers (MA_HP; n = 24; mean age ± SEM 54.2 ± 0.6-year-old) from low performers (MA_LP; n = 24; mean age ± SEM 54.3 ± 0.7-year-old) considering their scores in a visuo-spatial working memory (VSWM) task. Both MA groups were compared to young adults (YA, n = 24; mean age ± SEM = 22.7 ± 0.5-year-old). Electroencephalography (EEG) and pupillometry were recorded while participants performed the WM task. Our results showed that aging is accompanied by reduced pupil dilation peak. Yet, MA_HP exhibited prompt pupil dilation, comparable to YA, while MA_LP showed delayed and blunted pupil responses. Regarding EEG engagement index (EI), both MA groups exhibited significantly higher frontal EI than YA, while parietal EI was only increased in MA_HP compared to YA. Considering event related spectrum perturbation, aging was characterized by a loss of fronto-central and parietal theta event related depression (ERD) during the task. MA_HP distinguished themselves by parietal alpha and beta ERD during encoding and frontal theta, alpha and beta ERD during retention. Collectively, our data suggest that high WM performance in midlife depends on the flexible modulation of autonomic and cortical resources, potentially facilitating the attentional mobilization necessary for cognitive coping. These neurophysiological signatures allow clearer distinction between a chronological aging profile and a successful cognitive aging profile.