Concept-Aligned Neuronal Representation Transfer Across Brain States

Neuronal representations formed during a given experience (e.g. place cells) reinstate during subsequent consolidation of that experience despite changes in behavioral state (e.g. place cell replay during sleep). Pinpointing when consolidation of specific memories occurs, especially those formed during one-shot, naturalistic experiences, remains a grand challenge. Detecting such internally-generated reinstatement in humans is particularly challenging with current methods. These combined issues create a single-exposure transfer-and-evaluation problem, where representations learned from sparse neuronal recordings during initial experience poorly generalize for evaluation in states with substantially different distributions. Here, using intracranial microelectrode recordings comprising 452 curated single-neuron units from 13 neurosurgical participants across densely-labeled source (i.e. movie watching) and target states where labels remain sparse (i.e. vocalized memory recall) or unavailable (i.e. sleep), we address this problem using cross-state domain adaptation and held-out neuronal validation during sleep. We build participant-specific models using region-wise attention encoders trained with multi-label classification and contrastive alignment to learned concept embeddings. To improve adaptation across brain states, we introduce Recall-Adapted Sleep Alignment (RASA), which combines sleep-domain alignment with recall-based semantic regularization. Crucially, we leverage the rare presence of concept-selective neurons, known to reactivate during both perceptually driven and internally generated reinstatement of their given concept, to test our decoding framework. Each reference neuron’s recording wire is excluded from model input throughout training, adaptation, and sleep evaluation. These neurons allow evaluation of decoding success during sleep by testing bidirectional temporal alignment between model-derived concept scores and their concept-selective activity even when behavioral labels are unavailable. Tested across 62 neurons selective to concepts during movie watching, RASA produces sleep-time concept scores that are more strongly concentrated around concept-matched held-out neuronal events and more precisely aligned with their timing than those from the movie-trained baseline and alternative neural decoders, providing evidence of sleep-time concept-aligned structure consistent with concept-specific reinstatement. We provide a general framework for transferring concept-aligned representations under severe cross-state distribution shift.