Life on the Edge: Insights into the Neural and Behavioral Algorithms of Plume Tracking

Author

Andrew Siliciano

Date of Award

2023

Document Type

Thesis

Degree Name

Doctor of Philosophy (PhD)

RU Laboratory

Ruta Laboratory

Abstract

Animals use turbulent odor plumes as chemical beacons to navigate long distances. What are the neural and behavioral algorithms that underlie such a navigational feat? While plume navigation has been conventionally described as a simple sensory reflex, animals may instead rely on their memories of past plume encounters and current assessment of the wind direction to pursue a dynamic odor source. Differentiating between these strategies has been challenging due to the fact that plumes are invisible and spatially complex, precluding an understanding of the exact sensory experience of an animal. We have been leveraging the concise architecture of the Drosophila olfactory and navigational circuitry to elucidate the neural mechanisms underlying odor navigation. We developed a virtual reality environment compatible with two-photon functional imaging that allows a walking head-fixed fly to navigate naturalistic odor landscapes, offering unique insight into the sensory signals and behavioral algorithms animals use for navigation. We find that flies track an appetitive odor plume by ascending upwind along its boundaries through a repeated pattern of upwind counter-turning inside and biased local exploration outside of the plume, a robust navigational strategy we term edge-tracking. Through modeling and behavioral perturbations of the fictive olfactory environment, we demonstrate that edge-tracking represents a form of spatial navigation in which flies must continually remember the direction of the plume’s boundary. Using calcium imaging and optogenetic perturbations of specific neuronal populations, we reveal that edge-tracking relies on the mushroom body and central complex, two highly interconnected brain centers implicated in olfactory learning and spatial navigation. In particular, the ongoing activity of dopaminergic neurons of the mushroom body previously implicated in associative learning shapes edge-tracking behavior over multiple timescales and is necessary for continued pursuit of the plume. Moreover, compass neurons within the central complex, a navigational center, carry a high-fidelity representation of the animal’s heading relative to the wind direction, and inhibiting these neurons prevents flies from remembering the location of the plume’s boundary. Together our work suggests how ongoing neuromodulation ultimately shapes navigational performance by reinforcing sensory, spatial or motor actions necessary to return to the plume’s edge. These studies highlight that instead of relying on simple sensory reflexes, flies use their sophisticated learning and navigational circuitry to track odor plumes, a feature likely to be shared between insect and mammalian brains.

Comments

A Thesis Presented to the Faculty of The Rockefeller University in Partial Fulfillment of the Requirements for the degree of Doctor of Philosophy

Recommended Citation

Siliciano, Andrew, "Life on the Edge: Insights into the Neural and Behavioral Algorithms of Plume Tracking" (2023). Student Theses and Dissertations. 733.
https://digitalcommons.rockefeller.edu/student_theses_and_dissertations/733