Garcia Huescar, M. | bioRxiv Science

bioRxiv2026

Hippocampal and Midbrain Function in Superagers Relates to Memory for Novelty and Expectation Violation

Memory performance typically declines with age, but the underlying neurobiological mechanisms remain unclear. Superagers, people over 80 years of age with episodic memory performance comparable to individuals 30 years younger, appear to resist this decline. Novelty and expectation violations are known to engage the hippocampus-midbrain system to enhance memory formation. Here, we examined whether superagers superior memory performance is supported by preserved hippocampal-midbrain function during novelty and expectation processing. We manipulated item and contextual novelty (i.e., expectation violations) during encoding to test whether superagers show greater mnemonic benefits than their age-matched peers, whether these benefits reflect enhanced hippocampal and midbrain functioning as measured by fMRI, and whether they are associated with preserved dopaminergic integrity measured with neuromelanin-sensitive MRI. Our results show that, although superagers demonstrated overall superior memory performance, both groups exhibited superior recognition of contextually unexpected items. Nevertheless, differences emerged in the processing of expectation during encoding. Superagers exhibited stronger hippocampal responses to expectation violations and habituation to expected events, irrespective of item novelty. Conversely, typical older adults exhibited reduced midbrain response when expected novelty was absent. Neuromelanin accumulation did not account for group differences in midbrain activity or memory performance. Taken together, these findings suggest superagers benefit from adaptive responses to expectation and its violation, which is therefore a candidate mechanism distinguishing exceptional from typical cognitive ageing. SIGNIFICANCE STATEMENTAlthough memory typically declines with age, superagers are individuals aged over 80 who maintain memory performance comparable to people 30 years younger. We examined whether preserved hippocampal-midbrain function during novelty and expectation processing could underlie their superior memory. Superagers exhibited adaptive hippocampal responses to expectation and its violation, with higher activation for unexpected events and habituation to expected events. In contrast, typical older adults showed hippocampal and midbrain responses oriented towards anticipated novel content, despite not showing differences in neuromelanin accumulation. These findings underscore the critical role of hippocampal function in supporting memory preservation in late life and advance our understanding of the neural mechanisms underlying healthy cognitive ageing.

neuroscience↗

bioRxiv2018

Cardiac afferent activity modulates early neural signature of error detection during skilled performance

Behavioral adaptations during performance rely on predicting and evaluating the consequences of our actions through action monitoring. Previous studies revealed that proprioceptive and exteroceptive signals contribute to error-monitoring processes, which are implemented in the posterior medial frontal cortex. Interestingly, errors trigger changes in autonomic nervous system activity such as pupil dilation or heartbeat deceleration. Yet, the contribution of implicit interoceptive signals of bodily states to error-monitoring during ongoing performance has been overlooked. This is more surprising given the evidence on the relevance of interoceptive signals for the modulation of perceptual, affective and cognitive processes.\n\nWe investigated whether cardiovascular interoceptive signals influence the neural correlates of error processing during performance, with an emphasis on the early stages of error processing. We recorded participants electroencephalography and electrocardiogram during the performance of highly-trained music pieces in musicians. Previous event-related potential (ERP) studies revealed that pitch errors during skilled musical performance are preceded by an error detection signal, the pre-error-negativity (preERN), and followed by a later error positivity (PE). In this study, by combining ERP, source localization and multivariate pattern classification analysis, we found that the error-correct ERP waveform had a larger amplitude within 40-100 ms following errors in the systolic period of the cardiac cycle. This component could be decoded from single-trials, was dissociated from the preERN and PE, and stemmed from the inferior parietal cortex, which is a region implicated in cardiac autonomic regulation. In addition, the cardiac phase influenced behavioral alterations resulting from errors, with a smaller post-error slowing and less perturbed velocity in keystrokes following pitch errors in the systole phase of the cardiac cycle. This study provides the first evidence of preconscious visceral information modulating neural and behavioral responses related to early error monitoring during skilled performance.

neuroscience↗