Input density tunes Kenyon cell sensory responses in the Drosophila mushroom body

• Published in: Current biology 2023-07, Vol.33 (13), p.2742-2760.e12
• Main Authors: Ahmed, Maria, Rajagopalan, Adithya E., Pan, Yijie, Li, Ye, Williams, Donnell L., Pedersen, Erik A., Thakral, Manav, Previero, Angelica, Close, Kari C., Christoforou, Christina P., Cai, Dawen, Turner, Glenn C., Clowney, E. Josephine
• Format: Article
• Language: English
• Subjects: Animals; brain engineering; development; Drosophila - physiology; Drosophila melangaster; Drosophila melanogaster - physiology; Drosophila Proteins - genetics; expansion layer; Marr-Albus theory; Mushroom Bodies - physiology; mushroom body; neural network; Neurons - physiology; Odorants; olfaction; pattern separation
• ISSN: 0960-9822; 1879-0445; 1879-0445
• DOI: 10.1016/j.cub.2023.05.064

The ability to discriminate sensory stimuli with overlapping features is thought to arise in brain structures called expansion layers, where neurons carrying information about sensory features make combinatorial connections onto a much larger set of cells. For 50 years, expansion coding has been a prime topic of theoretical neuroscience, which seeks to explain how quantitative parameters of the expansion circuit influence sensory sensitivity, discrimination, and generalization. Here, we investigate the developmental events that produce the quantitative parameters of the arthropod expansion layer, called the mushroom body. Using Drosophila melanogaster as a model, we employ genetic and chemical tools to engineer changes to circuit development. These allow us to produce living animals with hypothesis-driven variations on natural expansion layer wiring parameters. We then test the functional and behavioral consequences. By altering the number of expansion layer neurons (Kenyon cells) and their dendritic complexity, we find that input density, but not cell number, tunes neuronal odor selectivity. Simple odor discrimination behavior is maintained when the Kenyon cell number is reduced and augmented by Kenyon cell number expansion. Animals with increased input density to each Kenyon cell show increased overlap in Kenyon cell odor responses and become worse at odor discrimination tasks. [Display omitted] •Odor representation in Kenyon cells is robust to changes in Kenyon cell number•Altering Kenyon cell input density tunes the sparsity of their odor responses•Mushroom body output neurons functionally accommodate changes to Kenyon cells•Odor discrimination behavior correlates with changes in Kenyon cell odor responses Ahmed et al. perturb mushroom body hard-wiring to test the Marr-Albus theory of pattern separation. By altering the number of Kenyon cells or their input density, they find that input density determines the sparsity of odor responses. Discrimination behavior is enhanced by increasing Kenyon cell number and degraded by making odor responses promiscuous.