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

Abstract

Ants communicate via large arrays of pheromones and possess expanded, highly complex olfactory systems, with antennal lobes in the brain comprising ~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 the first transgenic ants, expressing the genetically encoded calcium indicator GCaMP6s 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 representation of alarm pheromone cues. 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.

Unselfish meiotic drive maintains heterozygosity in a parthenogenetic ant

“…We detected dsRed and autofluorescence by imaging brains and gasters using the red and green fluorescence channels of an epifluorescence microscope (Supplementary Figure 2). While individuals from a previous study with [ie1-dsRed, ObirOrco-QF2, 15xQUAS-GcaMP6s] express dsRed in their antennal lobes 32 , fluorescence is not visible in dissected brains of ants with ie1-dsRed alone. This suggests that the ie1 promoter does not normally drive expression in brain tissue, but interaction between adjacent transgenes can lead to leaky expression 32 .…”

“…For this, we used a plasmid with a piggyBac backbone to transpose the baculovirus-derived ie1 enhancer/promoter element to drive expression of the red fluorescent protein dsRed (Supplementary Figure 2). This plasmid (pBac-ie1-dsRed) was assembled as part of a previous study 32 . For transgenesis, we collected 660 eggs from clonal line B 13,33 , injected them with pBac-ie1-dsRed, and reared the resulting fluorescent individuals according to our established protocol 32 , yielding isogenic colonies of fluorescent individuals derived from single founders.…”

Pheromone representation in the ant antennal lobe changes with age

“…Such changes might be detectable by recording odor-evoked calcium responses in the AL, where olfactory sensory neuron (OSN) axons synapse with central brain neurons to form glomeruli ( 20 ). In a previous study, we used volumetric two-photon microscopy to image whole-AL odor responses in ants expressing GCaMP6s specifically in OSNs (“GCaMP6s ants”) ( 18 ). Here, we applied the same approach to study putative differences in neural function between young and old ants.…”

“…Similar to other social insects ( 11 , 12 , 16 ), older ants responded more rapidly to alarm pheromones, the chemical signals for danger. Using whole-AL calcium imaging ( 18 ), we then mapped odor representations for five general odorants and two alarm pheromones in young and old ants. Alarm pheromones were represented sparsely at all ages.…”

Synergistic olfactory processing for social plasticity in desert locusts

“…To some degree, these differences can account for potential disparities between odor coding in the locust literature -described as temporally evolving trajectories (recorded electrophysiologically from PN somata,Anton et al (2002);Mazor and Laurent (2005);Saha et al (2015)), and the fruit fly and honeybee literature -describing more transient combinatorial patterns (recorded primarily via functional imaging from the dendritic terminals, e.g.,Sachse and Galizia (2003);Vosshall et al (2000)). Recent observations from clonal raider ants -another insect species with largely arborized ALs, similar to locusts -revealed a highly stereotyped odor encoding logic in the ORN population(Hart et al (2023)). As odor discrimination and coding efficiency are predicted to be preserved and even enhanced at the postsynaptic layer of PNs(Bhandawat et al (2007);Lüdke et al (2018);Raman et al (2010)),…”