TY - JOUR TI - A dentate gyrus-CA3 inhibitory circuit promotes evolution of hippocampal-cortical ensembles during memory consolidation AU - Twarkowski, Hannah AU - Steininger, Victor AU - Kim, Min Jae AU - Sahay, Amar A2 - Cai, Denise A2 - Colgin, Laura L A2 - de la Prida, Liset M VL - 11 PY - 2022 DA - 2022/02/22 SP - e70586 C1 - eLife 2022;11:e70586 DO - 10.7554/eLife.70586 UR - https://doi.org/10.7554/eLife.70586 AB - Memories encoded in the dentate gyrus (DG) ‒ CA3 circuit of the hippocampus are routed from CA1 to anterior cingulate cortex (ACC) for consolidation. Although CA1 parvalbumin inhibitory neurons (PV INs) orchestrate hippocampal-cortical communication, we know less about CA3 PV INs or DG ‒ CA3 principal neuron ‒ IN circuit mechanisms that contribute to evolution of hippocampal-cortical ensembles during memory consolidation. Using viral genetics to selectively mimic and boost an endogenous learning-dependent circuit mechanism, DG cell recruitment of CA3 PV INs and feed-forward inhibition (FFI) in CA3, in combination with longitudinal in vivo calcium imaging, we demonstrate that FFI facilitates formation and maintenance of context-associated neuronal ensembles in CA1. Increasing FFI in DG ‒ CA3 promoted context specificity of neuronal ensembles in ACC over time and enhanced long-term contextual fear memory. In vivo LFP recordings in mice with increased FFI in DG ‒ CA3 identified enhanced CA1 sharp-wave ripple ‒ ACC spindle coupling as a potential network mechanism facilitating memory consolidation. Our findings illuminate how FFI in DG ‒ CA3 dictates evolution of ensemble properties in CA1 and ACC during memory consolidation and suggest a teacher-like function for hippocampal CA1 in stabilization and re-organization of cortical representations. KW - hippocampus KW - systems consolidation KW - dentate gyrus KW - CA3 KW - parvalbumin inhibitory interneuron KW - calcium imaging KW - Anterior cingulate cortex KW - ripples KW - spindles KW - ensemble KW - memory KW - LFPs JF - eLife SN - 2050-084X PB - eLife Sciences Publications, Ltd ER -