Structural spine plasticity: learning and forgetting of odor-specific subnetworks in the olfactory bulb

Abstract

Learning to discriminate between different sensory stimuli is essential for survival. In rodents, the olfactory bulb, which contributes to odor discrimination via pattern separation, exhibits extensive structural synaptic plasticity involving the formation and removal of synaptic spines, even in adult animals. The network connectivity resulting from this plasticity is still poorly understood. To gain insight into this connectivity we present here a computational model for the structural plasticity of the reciprocal synapses between the dominant population of excitatory principal neurons and inhibitory interneurons. It incorporates the observed modulation of spine stability by odor exposure. The model captures the striking experimental observation that the exposure to odors does not always enhance their discriminability: while training with similar odors enhanced their discriminability, training with dissimilar odors actually reduced the discriminability of the training stimuli (Chu et al, 2016). Strikingly, this differential learning does not require the activity-dependence of the spine stability and occurs also in a model with purely random spine dynamics in which the spine density is changed homogeneously, e.g., due to a global signal. However, the experimentally observed odor-specific reduction in the response of principal cells as a result of extended odor exposure (Kato et al. 2012) and the concurrent disinhibition of a subset of principal cells arise only in the activity-dependent model. Moreover, this model predicts the experimentally testable recovery of odor response through weak but not through strong odor re-exposure and the forgetting of odors via exposure to interfering odors. Combined with the experimental observations, the computational model provides strong support for the prediction that odor exposure leads to the formation of odor-specific subnetworks in the olfactory bulb. Author SummaryA key feature of the brain is its ability to learn through the plasticity of its network. The olfactory bulb in the olfactory system is a remarkable brain area whose anatomical structure evolves substantially still in adult animals by establishing new synaptic connections and removing existing ones. We present a computational model for this process and employ it to interpret recent experimental results. By comparing the results of our model with those of a random control model we identify various experimental observations that lend strong support to the notion that the network of the olfactory bulb comprises learned, odor-specific subnetworks. Moreover, our model explains the recent observation that the learning of odors does not always improve their discriminability and provides testable predictions for the recovery of odor response after repeated odor exposure and for when the learning of new odors interferes with retaining the memory of familiar odors.