Decoding peripheral stimulation from cortical and spinal recordings reveals complementary sensorimotor information
Toni, L.; Caffi, G.; Mazzarino, A.; Nierula, B.; Emedoli, D.; Agnesi, F.; Iannaccone, S.; Artoni, F.; Micera, S.
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The somatosensory system encodes peripheral inputs through a sequence of ascending neural relays spanning spinal, subcortical and cortical levels. While multivariate decoding of electroencephalography (EEG) signals has demonstrated that cortical activity contains fine-grained information about somatosensory stimuli, the extent to which earlier processing stages contribute additional, non-redundant information remains unclear. To address this gap, we investigated a dataset comprising peripheral sensory stimulation and mixed stimulation (i.e., stimulation engaging both sensory and motor fibers). We assessed whether stimulation characteristics can be decoded from spinal recordings using high-density electrospinography (ESG), and whether combining ESG with EEG enhances decoding performance. Decoding accuracy varied systematically with both stimulation type and signal modality. ESG was the most informative signal for mixed and mixed vs sensory discrimination, reaching an average accuracy of [~]98%, while EEG provided a relative advantage for purely sensory tasks, though absolute accuracy remained more modest for both modalities. Critically, combining the two modalities together consistently matched or outperformed either one, used alone, across all conditions, with gains most pronounced for mixed vs sensory discrimination. Multi-subject generalization improved progressively with training-set size, rising to [~]88% with 15 training subjects for mixed classification, suggesting that subject-independent decoding of motor intent may be achievable when models are trained on a larger number of subjects. Taken together, these results establish that spinal ESG signals carry decodable information about peripheral stimulation that is complementary to and not redundant with cortical EEG. This finding supports a multilevel framework for decoding sensorimotor processing in humans and motivates the development of dual-modality brain-machine interfaces that leverage both cortical and spinal signals to improve the control of neurostimulation and assistive devices.
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