Idiosyncratic neural coding and neuromodulation of olfactory individuality in Drosophila

K. Honegger,M. A. Smith,M. Churgin,Glenn C. Turner,Benjamin L. de Bivort

Published 2019 in Proceedings of the National Academy of Sciences of the United States of America

ABSTRACT

Significance Individuality is a fundamental feature of behavior. For instance, the same smell or song may evoke very different responses in 2 individuals. What is the biological basis for these differences? While behavioral differences likely originate with differences in neural activity, little is known about how idiosyncratic behavioral differences are reflected in neural activity. We used statistical behavioral analysis and live brain imaging to assess idiosyncratic odor responses in fruit flies, and found that the same odors produce different behavioral responses across flies and that these odors evoke subtly different patterns of brain activity across flies. Moreover, neuromodulators and sets of neurons in the olfactory region of the fly’s brain directly modulate the degree of fly-to-fly behavioral variability in a flexible way. Innate behavioral biases and preferences can vary significantly among individuals of the same genotype. Though individuality is a fundamental property of behavior, it is not currently understood how individual differences in brain structure and physiology produce idiosyncratic behaviors. Here we present evidence for idiosyncrasy in olfactory behavior and neural responses in Drosophila. We show that individual female Drosophila from a highly inbred laboratory strain exhibit idiosyncratic odor preferences that persist for days. We used in vivo calcium imaging of neural responses to compare projection neuron (second-order neurons that convey odor information from the sensory periphery to the central brain) responses to the same odors across animals. We found that, while odor responses appear grossly stereotyped, upon closer inspection, many individual differences are apparent across antennal lobe (AL) glomeruli (compact microcircuits corresponding to different odor channels). Moreover, we show that neuromodulation, environmental stress in the form of altered nutrition, and activity of certain AL local interneurons affect the magnitude of interfly behavioral variability. Taken together, this work demonstrates that individual Drosophila exhibit idiosyncratic olfactory preferences and idiosyncratic neural responses to odors, and that behavioral idiosyncrasies are subject to neuromodulation and regulation by neurons in the AL.

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