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NeurosciencebioRxiv
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Unconstrained naturalistic human brain imaging and decoding with a fully wearable high-density optical system

William T. HamiciD, Wiete FehneriD, Morgan FogartyiD, Alvin AgatoiD, Hannah E. DeVoreiD, Sean M. RaffertyiD, Dana Wilhelm, Amelia M. HinesiD, Adam T. EggebrechtiD, Jason W. TrobaughiD, Edward J. RichteriD, Joseph P. CulveriD

Abstract

Understanding how the brain supports complex cognition in real-world environments requires neuroimaging systems that impose minimal constraints on natural behavior. Existing high-fidelity modalities, such as functional magnetic resonance imaging (fMRI), confine participants to the scanner, while wearable alternatives sacrifice spatial resolution or cortical coverage. Here, we developed a fully untethered whole-head optical neuroimaging system that achieves high-fidelity tomographic reconstruction through dense spatial sampling, configurable source multiplexing, and high dynamic range detection. This wearable high-density diffuse optical tomography (WHD-DOT) system achieves 151 dB effective dynamic range and nearly 3000 source-detector measurements, comparable to the highest-performing fiber-based DOT systems, while maintaining wireless, battery-powered mobility. We validate WHD-DOT across three paradigms of increasing ecological complexity, ranging from standard functional localizers to naturalistic movie viewing and live piano performance. Across all paradigms, WHD-DOT produces robust, well-localized encoding, repeatable single-trial responses, and above-chance decoding of stimulus-specific dynamics. Piano performance, which requires continuous bimanual movement and an unconstrained posture, is a rigorous real-world test for a wearable neuroimaging system. By decoding song-segment identity of free piano performance at 71.1% accuracy (chance 12.5%), WHD-DOT shows that brain activity from unconstrained, real-world behavior, previously beyond reach of high-fidelity imaging, is now both measurable and decodable.

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