Abstract
<jats:title>Abstract</jats:title> <jats:p>Episodic-memory impairment is a defining feature of Mild cognitive impairment (MCI), yet the large-scale neural processes through which medial temporal pathology translates into poor cognitive performance remain unclear. Fast brain activity can be organized into transient, aperiodic bursts—neuronal avalanches—that propagate from hippocampal and adjacent temporal regions across distributed brain networks, potentially indexing interactions relevant to memory. We therefore hypothesized that episodic-memory impairment in MCI reflects an altered ability of the temporal pole to initiate these activity cascades. We analyzed resting-state, source-reconstructed MEG recordings from 29 individuals with MCI and 32 healthy controls (HC). Large-scale dynamics were described in terms of neuronal avalanches, and we quantified each temporal-pole region’s propensity to act as an “avalanche starter” —that is, to be the first region to become active. We then related this measure to episodic-memory performance and hippocampal volume. Although temporal-pole starter frequency did not differ between groups, its relationship with memory performance was reversed. Greater avalanche initiation from the left temporal pole was associated with poorer memory performance in MCI, as measured by the delayed free recall in the Free and Cued Selective Reminding Test. The same relationship was positive in HC. Within the MCI group, greater left-temporal-pole starter frequency was also associated with hippocampal atrophy. These findings suggest that MCI involves a qualitative reorganization of temporal-pole–initiated dynamics rather than a simple change in their frequency. This framework links local structural vulnerability to altered whole-brain dynamics and episodic-memory impairment.</jats:p> <jats:sec> <jats:title>Significance Statement</jats:title> <jats:p>Memory decline is a hallmark of Mild Cognitive Impairment (MCI), often a precursor to Alzheimer’s disease, yet how the brain’s large-scale dynamics change to produce this decline remains unclear. Using magnetoencephalography, we studied brief bursts of coordinated activity — neuronal avalanches — and introduced the “avalanche starter”: a region’s propensity to initiate, rather than join, one of these cascades. We focused on the temporal pole, among the earliest regions affected by Alzheimer’s pathology. In healthy adults, frequent avalanche initiation there was linked to better memory; in MCI, the same pattern was linked to worse memory and hippocampal atrophy. This reversal shows that early cognitive decline reflects a qualitative reorganization of temporal-pole-driven dynamics, rather than a simple change in activity levels.</jats:p> </jats:sec>