Sparse and stereotyped encoding implicates a core glomerulus for ant alarm behavior

Taylor Hart; Dominic D Frank; Lindsey E Lopes; Leonora Olivos-Cisneros; Kip D Lacy; Waring Trible; Amelia Ritger; Stephany Valdés-Rodríguez; Daniel J C Kronauer

doi:10.1016/j.cell.2023.05.025

Sparse and stereotyped encoding implicates a core glomerulus for ant alarm behavior

Cell. 2023 Jul 6;186(14):3079-3094.e17. doi: 10.1016/j.cell.2023.05.025. Epub 2023 Jun 14.

Authors

Taylor Hart¹, Dominic D Frank², Lindsey E Lopes², Leonora Olivos-Cisneros², Kip D Lacy², Waring Trible³, Amelia Ritger⁴, Stephany Valdés-Rodríguez⁵, Daniel J C Kronauer⁶

Affiliations

¹ Laboratory of Social Evolution and Behavior, The Rockefeller University, 1230 York Avenue, New York, NY 10065, USA. Electronic address: thart@rockefeller.edu.
² Laboratory of Social Evolution and Behavior, The Rockefeller University, 1230 York Avenue, New York, NY 10065, USA.
³ Laboratory of Social Evolution and Behavior, The Rockefeller University, 1230 York Avenue, New York, NY 10065, USA; John Harvard Distinguished Science Fellowship Program, Harvard University, 52 Oxford Street, NW Cambridge, MA 02138, USA.
⁴ Laboratory of Social Evolution and Behavior, The Rockefeller University, 1230 York Avenue, New York, NY 10065, USA; Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, Marine Science Research Building, Bldg. 520, Santa Barbara, CA 93106, USA.
⁵ Laboratory of Social Evolution and Behavior, The Rockefeller University, 1230 York Avenue, New York, NY 10065, USA; Howard Hughes Medical Institute, New York, NY 10065, USA.
⁶ Laboratory of Social Evolution and Behavior, The Rockefeller University, 1230 York Avenue, New York, NY 10065, USA; Howard Hughes Medical Institute, New York, NY 10065, USA. Electronic address: dkronauer@rockefeller.edu.

Abstract

Ants communicate via large arrays of pheromones and possess expanded, highly complex olfactory systems, with antennal lobes in the brain comprising up to ∼500 glomeruli. This expansion implies that odors could activate hundreds of glomeruli, which would pose challenges for higher-order processing. To study this problem, we generated transgenic ants expressing the genetically encoded calcium indicator GCaMP in olfactory sensory neurons. Using two-photon imaging, we mapped complete glomerular responses to four ant alarm pheromones. Alarm pheromones robustly activated ≤6 glomeruli, and activity maps for the three pheromones inducing panic alarm in our study species converged on a single glomerulus. These results demonstrate that, rather than using broadly tuned combinatorial encoding, ants employ precise, narrowly tuned, and stereotyped representations of alarm pheromones. The identification of a central sensory hub glomerulus for alarm behavior suggests that a simple neural architecture is sufficient to translate pheromone perception into behavioral outputs.

Keywords: GCaMP; Ooceraea biroi; antennal lobe; calcium imaging; chemosensation; clonal raider ant; communication; odor coding; olfaction; pheromone.

Publication types

Research Support, N.I.H., Extramural
Research Support, U.S. Gov't, Non-P.H.S.
Research Support, Non-U.S. Gov't

MeSH terms

Animals
Ants* / genetics
Behavior, Animal
Brain / physiology
Odorants
Pheromones
Smell / physiology

Substances

Pheromones

Abstract

Publication types

MeSH terms

Substances

Grants and funding