Decomposing representational drift across wake and sleep

Abstract

Neural representations evolve over time, yet the relative contributions of online experience and offline states such as sleep remain unclear. Here, we recorded single-unit activity in the olfactory cortex of mice across cycles of awake odour exposure and sleep, and developed a low-rank decoder to track representational drift. We identified four orthogonal drift modes operating on distinct timescales, revealing that sleep and wake drive qualitatively different transformations, which indicates that offline reorganisation is not a simple continuation of online learning. Rather, sleep initiates an about-turn in the overall drift trajectory, which is uniquely characterised by a combination of decorrelation and rotation of odour representations. We also provide the first evidence for olfactory replay, occurring at ~2.5x temporal compression and associated with locally generated piriform cortex sharp waves. Together, these findings demonstrate that representational drift comprises state-dependent components, and reveal distinct contributions of wake and sleep to sensory representational change.