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

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

doi:10.1016/j.cell.2023.05.025

Cited by 18 publications

(27 citation statements)

References 128 publications

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“…We examined whether clonal raider ants show age-dependent plasticity in alarm behavior using a colony bioassay. Upon stimulation with alarm pheromones, the ants begin to move quickly and disassemble the nest pile where the eggs are located (17,18). Clonal raider ants can live for up to a year (19), so we selected "young ants" (two weeks old) and "old ants" (two months old) to examine effects of age while excluding effects of senescence.…”

Section: Resultsmentioning

confidence: 99%

“…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.…”

Section: Resultsmentioning

confidence: 99%

“…Next, we imaged AL responses in young and old GCaMP6s ants during stimulation with an odorant panel that evoked robust responses in our prior study at 3% and 48% concentration volume/volume in paraffin oil (alarm pheromones: 4-methyl-3-heptanone and 4-methyl-3heptanol; general odorants: 3-hexanone, isopropanol, ethylpyrazine, ethanol, and propionic acid) (18). Calcium responses to 4-methyl-3-heptanone and 4-methyl-3-heptanol were sparse at both tested ages, and total AL responses did not differ with age for either of the two tested concentrations (Fig.…”

Section: Resultsmentioning

confidence: 99%

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Pheromone representation in the ant antennal lobe changes with age

Hart,

Lopes,

Frank

et al. 2024

Preprint

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While the neural basis of age-related decline has been extensively studied (1–3), less is known about changes in neural function during the pre-senescent stages of adulthood. Adult neural plasticity is likely a key factor in social insect age polyethism, where individuals perform different tasks as they age and divide labor in an age-dependent manner (4–9). Primarily, workers transition from nursing to foraging tasks (5, 10), become more aggressive, and more readily display alarm behavior (11–16) as they get older. While it is unknown how these behavioral dynamics are neurally regulated, they could partially be generated by altered salience of behaviorally relevant stimuli (4, 6, 7). Here, we investigated how odor coding in the antennal lobe (AL) changes with age in the context of alarm pheromone communication in the clonal raider ant (Ooceraea biroi) (17). 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. However, alarm pheromone responses within individual glomeruli changed with age, either increasing or decreasing. Only two glomeruli became sensitized to alarm pheromones with age, while at the same time becoming desensitized to general odorants. Our results suggest that the heightened response to alarm pheromones in older ants occurs via increased sensitivity in these two core glomeruli, illustrating the importance of sensory modulation in social insect division of labor and age-associated behavioral plasticity.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

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Pheromone representation in the ant antennal lobe changes with age

Hart,

Lopes,

Frank

et al. 2024

Preprint

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“…, 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)), it is likely that, at least, a comparable level of odor separation will be observed by the PN population.…”

Section: Discussionmentioning

confidence: 99%

Synergistic olfactory processing for social plasticity in desert locusts

Petelski,

Günzel,

Sayin

et al. 2023

Preprint

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Desert locust plagues threaten the food security of millions. Central to their formation is crowding-induced social plasticity from solitarious to gregarious phenotypes. We investigated the impact of population density changes on locusts foraging choices and their neurobiology by examining how relevant food and social odors are coded in the antennal lobe. Our analysis shows that gregarious locusts are highly attentive to social cues during foraging, with olfaction playing an essential role. Using calcium imaging, we show that corresponding odors are encoded by projection neurons, revealing a stable combinatorial response map. Transient dynamics in the glomeruli converge into temporally evolving response motifs in the somata that differ between gregarious and solitarious insects. The dynamics of response motifs facilitate a crowding-dependent synergy between olfactory processing of food-related and social odors. Our study demonstrates the effectiveness of calcium imaging for locust olfaction, suggesting a crowding-induced adaptation to enhance food detection in swarms.

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“…Second, it was still difficult to deeply understand the neuronal circuits underlying the web-building behaviour. Advanced gene editing and neurobiological technology 59 will greatly improve our understanding of spider web-building behaviour.…”

Section: Genetic Drivers Of Neuron and Behaviour Innovation In Spidersmentioning

confidence: 99%

Single-cell transcriptomics reveals the brain evolution of web-building spiders

Jin,

Zhu,

Jia

et al. 2023

Nat Ecol Evol

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Spiders are renowned for their efficient capture of flying insects using intricate aerial webs. How the spider nervous systems evolved to cope with this specialized hunting strategy and various environmental clues in an aerial space remains unknown. Here we report a brain-cell atlas of >30,000 single-cell transcriptomes from a web-building spider (Hylyphantes graminicola). Our analysis revealed the preservation of ancestral neuron types in spiders, including the potential coexistence of noradrenergic and octopaminergic neurons, and many peptidergic neuronal types that are lost in insects. By comparing the genome of two newly sequenced plesiomorphic burrowing spiders with three aerial web-building spiders, we found that the positively selected genes in the ancestral branch of web-building spiders were preferentially expressed (42%) in the brain, especially in the three mushroom body-like neuronal types. By gene enrichment analysis and RNAi experiments, these genes were suggested to be involved in the learning and memory pathway and may influence the spiders’ web-building and hunting behaviour. Our results provide key sources for understanding the evolution of behaviour in spiders and reveal how molecular evolution drives neuron innovation and the diversification of associated complex behaviours.

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

Cited by 18 publications

References 128 publications

Pheromone representation in the ant antennal lobe changes with age

Pheromone representation in the ant antennal lobe changes with age

Synergistic olfactory processing for social plasticity in desert locusts

Single-cell transcriptomics reveals the brain evolution of web-building spiders

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