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. However, how these distinct representations emerge from the underlying local circuit architecture remains unknown. Using two-photon imaging of CA3 subareas during active behavior, we reveal opposing coding strategies within specific CA3 subregions, with proximal neurons demonstrating stable and generalized representations and distal neurons showing dynamic and context-specific activity. To test the causal role of excitatory connectivity in neural computation, we employed a genetic manipulation approach in which local disruption of glutamatergic synaptic transmission 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 differences in coding properties to emerge. We confirmed the contribution of recurrent connectivity to functional heterogeneity by characterizing the representational geometry of neural recordings and comparing it with theoretical predictions of neural manifold dimensionality. 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. HighlightsO_LIProximodistal CA3 subregions implement complementary coding strategies in relation to time and context C_LIO_LIDisrupting excitatory recurrence in distal CA3 impairs context-discriminative neural coding C_LIO_LISparse and dense neural networks capture the functional heterogeneity of CA3 subcircuits C_LIO_LIRecurrence level tunes the geometry of neural manifolds both in vivo and in silico C_LI