When the inner clock fades: Interoceptive decline and consolidation of phase resetting in cortical rhythms by cardiac events underlie healthy lifespan aging.

Abstract

The brain continuously integrates signals from the external environment along with internal bodily cues to support adaptive cognition and homeostasis. Among these, multiple visceral rhythms, such as respiration, circadian fluctuations, and cardiac activity, contribute to the organization of intrinsic brain dynamics. The present study focuses on cardiac signals, as the heartbeat provides a continuous, quasi-periodic physiological rhythm that enables precise time-locking of neural responses and offers a tractable model for investigating brain-body interactions at rest. Interoceptive processing is influenced by factors, including arousal, emotional state, and aging, and is known to be altered in neurological conditions such as Parkinson's disease and dementia. Here, we investigated how the cortical representation of cardiac signals changes across the adult lifespan and the mechanisms underlying this reorganization. Using a large human cohort (N = 620, aged 18-88 years) with simultaneous resting-state MEG and ECG, the study found that cortical heartbeat-evoked responses (HERs) showed distinct amplitude changes in the 180-320 ms window post the heartbeat including a systematic reduction in amplitude with age. Cardiac signals modulated the phase of ongoing theta-band neural oscillations rather than altering overall power, and this phase-resetting effect became more consolidated in older adults. Source analysis revealed that resting-state HERs originated primarily from fronto-temporal regions, including orbitofrontal, frontal, and temporal pole areas, and exhibited a clear age-related shift from predominantly frontal to more temporal generators. Directed connectivity analyses revealed an age-related shift in heart-brain communication, characterized by increased heart-to-brain and decreased brain-to-heart Granger causality. Together, these findings demonstrate that cardiac processing undergoes systematic age-related reorganization, characterized by changes in response amplitude, phase dynamics, and heart-brain interactions. These alterations may contribute to broader age-related differences in cognitive functions such as attention, emotions, and time perception.