Prefrontal-thalamic goal states organize spatially aligned hippocampal maps.

Abstract

Animals repeatedly traverse the same environment to pursue different goals, yet the hippocampus must preserve a stable spatial map while keeping individual experiences distinct. Here we show that, when male rats navigate the same maze under different goal configurations, hippocampal CA1 segregates navigation experiences by encoding goal state along a population dimension largely orthogonal to the spatial coding subspace, allowing goal-configuration-specific maps to remain spatially aligned. This goal-state signal is also represented in the medial prefrontal cortex (mPFC) and nucleus reuniens (NR), where population activity forms persistent representations across locomotion and immobility and is reliably reinstated when previously experienced goal configurations recur. Silencing NR reduces CA1 goal-state coding, diminishing goal-axis separation and goal-biased pre-navigation spike sequences while sparing spatial coding. Together, these findings identify a circuit- and population-level mechanism that enables goal-defined hippocampal representations to coexist within spatially aligned maps independent of locomotor state, linking internal goal states to navigation and planning.