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A distributed neural architecture of sustained affect across external and internal experience

Ran ZhangiD, Debo DongiD, Xianyang GaniD, Sarah GenoniD, Simon Bodo EickhoffiD, Ting Xu, Bing CaoiD, Qinghua HeiD, Tingyong FengiD, Benjamin BeckeriD, Feng ZhouiD

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Abstract

AO_SCPLOWBSTRACTC_SCPLOWSustained affect shapes well-being, yet its neural architecture across externally elicited and internally generated experience remains unclear. Using whole-brain functional connectivity during minutes-long naturalistic movie viewing, we derived positive and negative affective experience signatures and their underlying neural architecture. These signatures predicted valence-specific affective intensity and generalized to independent movie-viewing data and internally generated affect, discriminating sad memory and rumination from neutral distraction while tracking subjective experience. Importantly, their expression showed little relation to vigilance or cognitive demand. Characterization of these signatures revealed coherent community structure and a shared distributed backbone, alongside valence-preferential components, consistent with a partially separable architecture. Extending beyond experimentally evoked states, in four resting-state depression cohorts, these signatures distinguished patients from controls with reduced positive and elevated negative signature expression, and predicted symptom burden and anhedonia. These findings identify a generalizable distributed architecture bridging external and internal affective experience and extending to clinically relevant affective dysregulation.

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