Dendritic processing of spontaneous neuronal sequences for one-shot learning

Spontaneous firing sequences colloquially called “preplay” are fundamental features of hippocampal network physiology. Preplay sequences have been hypothesized to participate in hippocampal learning and memory, but such functional roles and their potential cellular mechanisms remain unexplored. Here, we report a computational model based on the functional propagation of preplay sequences in the CA3 neuronal network. The model instantiates two synaptic pathways in CA3 neurons, one for proximal dendrite-somatic interactions to generate intrinsic preplay sequences and the other for distal dendritic processing of extrinsic sensory signals. The core dendritic computation is the maximization of matching between patterned activities in the two compartments through nonlinear spike generation. The model performs robust one-shot learning with long-term stability and independence that are modulated by the plasticity of dendrite-targeted inhibition. This model demonstrates that learning models combined with dendritic computations can enable preplay sequences to act as templates for rapid and stable memory formation.