Extinction reshapes SWR-coupled reactivation of behavior-defined assembly templates and auditory responses during...

Sleep supports memory processing, and hippocampal sharp-wave ripples (SWRs) are associated with the re-expression of waking population activity in hippocampal-cortical networks. However, how extinction training alters SWR physiology, SWR-coupled assembly activity, and sensory responsiveness during subsequent sleep remains unclear. Here, we recorded neuronal activity in hippocampal CA1 and auditory cortex (AC) in mice during sleep after overtraining and after extinction in a sound-guided T-maze task. Post-extinction sleep contained more SWRs, but these events showed lower ripple frequency and reduced sharp-wave amplitude. At the single-neuron level, CA1 pyramidal cells and interneurons displayed elevated firing during post-extinction sleep, whereas their SWR-evoked responses were reduced; in contrast, AC neurons showed enhanced SWR-evoked firing. Using assembly templates extracted from post-learned locomotor activity, we found that SWR-coupled expression of behavior-defined CA1 assembly templates was reduced during post-extinction sleep, whereas the corresponding expression of AC templates was enhanced. Additional representational-similarity, shuffle, dropout, and contribution analyses supported an assembly-level interpretation of these effects. In parallel, CA1 sound-suppressed neurons exhibited stronger baseline-corrected auditory responses during post-extinction sleep. Together, these findings indicate that extinction reshapes SWR physiology, redistributes hippocampal-cortical assembly expression, and alters auditory responsiveness during subsequent sleep.

The online version contains supplementary material available at 10.1007/s11571-026-10459-7.