Dissociation between impaired explicit spatial remapping and preserved implicit neural dynamics in Alzheimers disease

Abstract

The hippocampus supports spatial memory by dynamically integrating external sensory inputs with intrinsic neural circuit dynamics during novel experience. In Alzheimers disease (AD), despite impaired hippocampal spatial remapping, spatial learning and memory abilities can remain partially preserved, a phenomenon consistent with cognitive resilience (Gomez-Isla and Frosch 2022, Jia, Xu et al. 2025). However, the hippocampal ensemble coding patterns associated with these preserved learning and memory abilities remain remains unclear. We hypothesize that intrinsic temporal structures of neuronal firing continue to facilitate the encoding of new spatial information. Using the AppNL-G-F rat model, we longitudinally tracked hippocampal CA1 activity during a familiar-novel context alternating task. We found a dissociation between impaired explicit spatial coding and preserved implicit temporal coding in the AD hippocampal network. Explicit spatial coding was impaired, as place cells showed weak discrimination between distinct contexts and failed to improve with learning. In contrast, implicit temporal coding exhibited learning-dependent refinement, with cofiring dynamic becoming increasingly context-specific across long-term experience. Further analysis suggested that the enhancement of implicit cofiring may be associated with the increased consistency of neural ensemble reactivation during sharp wave ripples in awake rest. Taken together, these findings reveal an explicit-implicit dissociation in the AD hippocampal network, suggesting that the learning-dependent refinement of implicit temporal coding may support preserved learning capacity despite impaired spatial remapping.