Recurrent connectivity shapes spatial coding in hippocampal CA3 subregions

Stable and flexible neural representations of space in the hippocampus are crucial for navigating complex environments, yet how they emerge from the underlying local circuit architecture remains unknown. Using two-photon functional imaging in behaving mice, we reveal opposing coding strategies at both single-cell and population levels along the hippocampal CA3 transverse axis, with proximal CA3 (low recurrence) demonstrating stable representations and distal CA3 (high recurrence) showing dynamic and context-specific activity. To test the causal role of excitatory connectivity in neural computation, we locally disrupted glutamatergic synaptic transmission and found impaired context-specific spatial coding in distal CA3. Aligned with these experimental results, we show in artificial neural network models that varying the recurrence level causes these distinct coding properties to emerge. Our results indicate that local circuit organization, particularly recurrent connectivity among excitatory neurons, plays a key role in shaping complementary spatial representations within the hippocampus.