Longitudinal evidence for attenuated local-global deviance detection as a precursor of working memory decline

Abstract

From the perspective of predictive coding, normal aging is accompanied by decreased weighting of sensory inputs and increased reliance on predictions, resulting in the attenuation of prediction errors in older age. Recent EEG research further revealed that the age-related shift from sensorium to predictions is hierarchy-selective, as older brains show little reduction in lower-level but significant suppression in higher-level prediction errors. Moreover, the disrupted propagation of prediction errors from the lower-level to the higher-level seems to be linked to deficient maintenance of information in working memory. However, it is unclear whether the hierarchical predictive processing continues to decline with advancing age as working memory. Here we longitudinally followed a sample of 78 participants from three age groups (including seniors, adults, and adolescents) over three years’ time. Seniors exhibited largely preserved local processing (consisting of comparable MMN, delayed P3a, and comparable RON) but significantly compromised global processing (consisting of suppressed frontocentral negativity and suppressed P3b) in the auditory local-global paradigm. These electrophysiological responses did not change with the passing of time, unlike working memory which deteriorated with advancing age. Correlation analysis further showed that these electrophysiological responses signalling prediction errors are indicative of concurrent working memory. Moreover, there was a correlation between earlier predictive processing and later working memory but not between earlier working memory and later predictive processing. The temporal asymmetry suggested that the hierarchy-selective attenuation of prediction errors is likely a precursor of working memory decline.

Significance Statement

While predictive coding is postulated as a fundamental principle of brain function, little is known about its developmental trajectory in normal aging. This is in stark contrast with the large body of research on age-related decline in cognition such as working memory, which could be conceptualised as a derivative of the predictive coding mechanism. Here we provided longitudinal evidence that the hierarchy-selective attenuation of prediction errors manifests as a stable feature while working memory deteriorates with advancing age. Correlation analysis further suggested that the attenuation of prediction errors is likely a precursor of working memory decline, rendering it a potential predictor of working memory deterioration before any clinically relevant symptoms would manifest in the aging population.