Optimal sparse olfactory representations persist in a plastic network

Abstract

The neural representation of a stimulus is repeatedly transformed as it moves from the sensory periphery to deeper layers of the nervous system. Sparsening transformations are thought to increase the separation between similar representations, encode stimuli with great specificity, maximize storage capacity as associative memories, and provide an energy efficient instantiation of information in neural circuits. In the insect olfactory system, odors are initially represented in the periphery as a combinatorial code with simple temporal dynamics. Subsequently, in the antennal lobe this representation is transformed into a dense spatiotemporal activity pattern. Next, in the mushroom body Kenyon cells (KCs), the representation is dramatically sparsened. Then in mushroom body output neurons (MBONs), the representation takes on a new dense spatiotemporal format. Here, we develop a computational model to simulate this chain of olfactory processing from the receptor neurons to MBONs. We demonstrate that representations of similar odorants are maximally separated, measured by the distance between the corresponding MBON activity vectors, when KC responses are sparse and that the sparseness is maintained across variations in odor concentration by adjusting the feedback inhibition KCs receive. Different odor concentrations require different strength and timing of feedback inhibition for optimal processing. Further, in vivo, the KC-MBON synapse is highly plastic, and changes in synaptic strength after learning can change the balance of excitation and inhibition and may lead to a change in the distance between MBON activity vectors of two odorants for the same level of KC population sparseness. Thus, what is an optimal degree of sparseness before odor learning, could be rendered sub-optimal post learning. Here, we show, however, that synaptic weight changes caused by spike timing dependent plasticity increase the distance between the odor representations from the perspective of MBONs and do not lead to a concomitant change in the optimal sparseness. Author SummaryKenyon cells (KCs) of the mushroom body represent odors as a sparse code. When viewed from the perspective of follower neurons, mushroom body output neurons (MBONs), an optimal level of KC sparseness maximally separates the representations of odors. However, the KC-MBON synapse is highly plastic and may be potentiated or depressed by odor-driven experience that could, in turn, perturb the optimality formed by pre-synaptic circuits. Contrary to this expectation, we show that synaptic plasticity based on spike timing of pre- and postsynaptic neurons improves the ability of the system to distinguish between the representations of similar odors while preserving the optimality determined by pre-synaptic circuits.