Local circuit architecture facilitates the emergence of cellular feature selectivity in the cerebral cortex. In the hippocampus, a striking form of feature selectivity can be found in the spatial receptive fields of pyramidal ('place') cells. Indeed, much of our current understanding of hippocampal mnemonic operations comes from circuit level investigations of place cell ensembles in vivo, and from a largely disjunct body of work on microcircuit and cellular level information processing in vitro. To date, it thus remains largely unknown whether and how neuronal architecture at single-cell level (i.e. dendrites) and at mesocale levels (i.e. local inhibitory circuits) regulate the emergence of feature tuning in hippocampal neurons during memory encoding. Likewise, we know puzzlingly little about how the same neuronal architecture can in parallel support effective memory consolidation. To interrogate the dynamic interaction of individual hippocampal area CA1 pyramidal cells with their surrounding microcircuitry during spatial navigation, we used in vivo single-cell electroporation approach for monosynaptic retrograde tracing, single-cell optogenetics, and subcellular-resolution calcium and voltage imaging. In my talk I will summarize our recent results related to: (1) local circuit regulation of feature selectivity in CA1, (2) local circuit plasticity supporting flexible memory reactivation in hippocampal area CA3, and (3) dendritic signal integration and plasticity supporting feature tuning formation and consolidation in dendrites of CA1 pyramidal cells. Together these results support the emerging notion that cellular and microcircuit architecture enable flexible information processing and storage in cortical memory circuits.