Abstract

We consider the question of how sensory networks enable the detection of sensory stimuli in a combinatorial coding space. We are specifically interested in the olfactory system, wherein recent experimental studies have reported the existence of rich, enigmatic response patterns associated with stimulus onset and offset. This study aims to identify the functional relevance of such response patterns (i.e., what benefits does such neural activity provide in the context of detecting stimuli in a natural environment). We study this problem through the lens of normative, optimization-based modeling. Here, we define the notion of a low-dimensional latent representation of stimulus identity, which is generated through action of the sensory network. The objective of our optimization framework is to ensure high-fidelity tracking of a nominal representation in this latent space in an energy-efficient manner. It turns out that the optimal motifs emerging from this framework possess morphologic similarity with prototypical onset and offset responses observed in vivo in locusts (Schistocerca americana) of either sex. Furthermore, this objective can be exactly achieved by a network with reciprocal excitatory–inhibitory competitive dynamics, similar to interactions between projection neurons and local neurons in the early olfactory system of insects. The derived model also makes several predictions regarding maintenance of robust latent representations in the presence of confounding background information and trade-offs between the energy of sensory activity and resultant behavioral measures such as speed and accuracy of stimulus detection.

Original languageEnglish
Pages (from-to)3408-3423
Number of pages16
JournalJournal of Neuroscience
Volume40
Issue number17
DOIs
StatePublished - Apr 22 2020

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