Dendritic activity in CA3 place cell coding in familiar and novel environments
Dendrites of pyramidal neurons integrate different sensory inputs, and non-linear dendritic computations drive feature selective tuning and plasticity. Yet little is known about how dendrites themselves represent the environment, the degree to which they are coupled to their soma, and how that coupling is sculpted with experience. In order to answer these questions, we developed a novel preparation in which we image soma and connected dendrites in a single plane across days using in vivo two-photon microscopy. Using this preparation, we monitored spatially tuned activity in area CA3 of the hippocampus in head-fixed mice running on a linear track. We identified “place dendrites”, which can stably and precisely represent both familiar and novel spatial environments. Dendrites can display place tuning independent of their connected soma and even their sister dendritic branches, the first evidence for branch specific tuning in the hippocampus. In a familiar environment, tuned place cell soma become more decoupled from their dendrites compared to non-tuned soma. This relationship is absent in a novel environment, suggesting an experience dependent selective gating of dendritic spatial inputs. We then built a data-driven multicompartment computational model that could capture the experimentally observed correlations. Our model predicts that branch specific tuning confers flexibility of spatial tuning to place cells, while homogeneity of dendritic tuning promotes place field stability. These findings demonstrate that spatial representation is organized in a branch specific manner within dendrites of a hippocampal pyramidal cell. Further, spatial inputs from dendrites to soma are selectively and dynamically gated in an experience dependent manner, endowing both flexibility and stability to the cognitive map of space.