Synergistic olfactory processing for social plasticity in desert locusts

Inga Petelski, Yannick Günzel, Sercan Sayin, Susanne Kraus, Einat Couzin-Fuchs

Posted on: 8 April 2024 , updated on: 9 April 2024

Preprint posted on 15 September 2023

The smell of a movable feast: researchers investigate the neuronal basis of olfactory-mediated foraging behavior in locusts.

Selected by T. W. Schwanitz, Lukas Weiss

Categories: neuroscience


Locusts were one of the Biblical plagues of Egypt—since the advent of human agriculture, fear of these insects and their voracious appetites has echoed throughout religion and storytelling. They have the ability to aggregate into dense clouds that destroy whole harvests. In spite of our ancient enmity with these insects, however, it is only recently that we’ve begun to understand how and why they form such imposing swarms.

Locusts (in this study, Schistocerca gregaria) come in two forms: a solitary and a gregarious form. Solitary locusts are bright green in color and do not aggregate. Gregarious locusts, by contrast, have a bold yellow-black appearance and do form large swarms. Locusts that are reared in high densities become gregarious, while those reared at low densities become solitary. Little is known about differences in sensory abilities between these two forms.

Petelski, Günzel and colleagues wanted to understand the differences between these two locust phenotypes and in particular the way in which they both process odors in the brain. To do so, they turned to calcium imaging, a technique that makes it possible to visualize neuronal activity by adding proteins that fluoresce in the presence of calcium (which flows into a neuron when it fires). Compared with fruit flies, calcium imaging in the locust smell-processing center, the antennal lobe, is especially tricky: in fruit flies, neurons that respond to a given odor converge on a single spherical bundle of synapses called a glomerulus. Fruit flies have 51 of these olfactory glomeruli (Bates et al., 2020). By contrast, the glomeruli in locusts are organized in a radial pattern made up of over 1,000 microglomeruli (Fig. 2C).

The authors first established that odor plays a role in the aggregation of gregarious locusts; then, they observed gregarious and solitary locust brain activity when exposed to various biologically relevant odors. Finally, they attempted to wrangle sense out of the 1,000 plus little blobs of activity that came out of their calcium imaging data.

Fig. 2: calcium imaging of the locust antennal lobe. A-Civ Images of the locust antennal lobe, with Ci-iv showing different Z-stacks of projection neurons in green and olfactory sensory neurons. D shows an overview of the authors’ analysis pipeline. E-Gii show calcium image traces from gregarious animals on the left and solitary animals on the right.

Highlighted results

To establish that olfaction plays a more prominent role in gregarious locust behavior, the authors first conducted a behavioral assay where a single locust in an arena could freely choose between going to a container with leaves, a container with locusts, or a container with both. Importantly, these containers could have holes to allow the scent to dissipate, be transparent to let the trial locusts see its compatriots, or both. The authors found that scent played an especially prominent role in the decision-making process of the gregarious locusts. Using a GC-MS analysis of the leaves coupled with calcium imaging, the authors concluded that leaf alcohol acetate is the primary odor driving locust attraction to leaves and produces similar calcium traces to whole leaf odor.

Petelski, Günzel and colleagues then used calcium dye backfills to image the olfactory  projection neurons, capturing activity in the dendrites and somata when exposed to leaf alcohol acetate odor, locust odor, or both odors together, resulting in few key conclusions:

  1. Calcium imaging responses were consistent across trials within the same animal and across several animals. Individual response units (called granules in the paper) responded in a stable combinatorial way to the applied odors. Olfactory responses appear to function in a combinatorial code in locusts.
  2. Gregarious, but not solitary animals, showed higher calcium responses to the food cues (leaf/leaf alcohol acetate) when the social odor cue (locust smell) was in the mix. Gregarious animals have a higher proportion of mixture-specific olfactory units than solitary animals. Gregarious locusts respond to the coincidence of both social and food odors.
  3. The responses of projection neuron somata can be divided into different response motifs. An analysis of these motifs shows that there are more synergistic interactions in gregarious locusts. Projection neuron somata show a higher degree of response overlap and integration between social and food odor in gregarious locusts.
  4. The authors created a model that has 92% accuracy in determining if a locust was solitary or gregarious based on their projection neuron somata response motifs. Projection neuron response motifs can predict the locust phenotype.

Taken together, these results suggest that changes in locust gregarious olfactory responses versus solitary locust olfactory responses are due to a subtle reweighting of existing neuronal pathways and dynamics. The interaction between social and food odor encoding in the antennal lobe could play a role in shaping collective foraging decisions in locusts. Teasing apart these subtle interactions in locusts and in other insects will no doubt be enriching for the broader field of sensory processing.

Why we like this study

Calcium imaging is a challenging technique: preparations require a lot of effort, limiting sample sizes and magnifying the impacts of noise on the data. We therefore appreciated the authors’ attempts to wrangle meaning out of a tricky dataset, further complicated by the biological structure of the locust antennal lobe. We especially liked seeing the inclusion of an insect with a different antennal lobe Bauplan than many of the more commonly imaged insects.



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Author's response

Yannick  Günzel and Einat Couzin-Fuchs shared

1. What are some future directions for this research? Do single glomeruli mean anything to these locusts, and how should we think about odor mapping in their antennal lobe?

We want to understand what makes locusts swarm and the neural processes associated with that. The adaptation to crowding and swarm-formation involves many molecular and neural processes which we so far know little about. The relatively shallow and accessible architecture of the olfactory circuits (probably the most studied brain region in locusts) makes the olfactory system a great candidate for high-resolution analysis of the neural processes mediating the behavioral shift. In addition, we also wonder whether the large expansion of the locust AL (in comparison with other circuits) in which odors are mapped by a broad population code can be advantageous for their extreme adaptability to environmental and population fluctuations. For instance, gregarious locusts display increased generalism regarding host plants during migrations, for which odor flexibility is key. So far we know little about the contribution of single glomeruli, yet drawing on a substantial body of previous work (i.e., Laurent 2002, Stopfer et al. 2003, Nizampatnam et al. 2018) and supported by our imaging data, we strongly believe odors to be encoded and decoded by a flexible population response.

2. What do the locusts smell like? Is there a single compound that captures the essence of locust smell in the way a single compound from leaf odor can evoke similar responses in the locust antennal lobe? Would it be easier to use just this compound moving forward, or is the locust smell more combinatorial?

Chemical analysis of locust volatiles in another major swarming species, the migratory locust, identified a few components, some of which are also specific to, or more pronounced in, the gregarious morph (Wei et al. 2017, Chang et al. 2023). Chemical profiling of the desert locust so far didn’t highlight single dominant components (except for those related to mating in mature adults), and we, therefore, used in our study the full colony blend. Moving forward, such an analysis can certainly be extremely beneficial for tracing phenotypic changes in specific parts of the network (i.e., local neurons and expression profiles of the receptors and peptides wiring the AL network). Nevertheless, it is also likely that the synergistic mixture processing described here is specially tuned for complex blends rather than specific compounds.

3. Does the locust visual system gate their olfactory system, or vice versa? Could you speculate (or do you perhaps have additional data) on why solitary locusts might not rely on odor as much as gregarious ones?

The hierarchies and interplay between the systems is a fascinating topic we are very much interested in exploring. It is also highly context-dependent; For example, in our field experiments, we noticed that during group marching locusts disregard olfactory cues and mainly rely on vision to determine traveling direction, while the evaluation of nearby food sources requires both. One potential explanation for the lack of clear solitarious response to the ‘locust smell’ seen here could be that it is evaluated as a novel odor with a weak intrinsic valance due to lack of previous exposure.

Generally, it would be fascinating to further explore the integration of different information classes on a neuronal level to corroborate our model’s predictions. In mosquitoes, for example, the processing of visual information is affected by the olfactory context (Vinauger et al. 2019, Alonso San Alberto et al. 2022, Barredo et al. 2022) and we are curious about similar mechanisms during the formation and progression of devastating locust swarms.


Alonso San Alberto, D., Rusch, C., Zhan, Y., Straw, A. D., Montell, C., & Riffell, J. A. (2022). The olfactory gating of visual preferences to human skin and visible spectra in mosquitoes. Nature communications, 13(1), 555.

Barredo, E., Raji, J. I., Ramon, M., DeGennaro, M., & Theobald, J. (2022). Carbon dioxide and blood-feeding shift visual cue tracking during navigation in Aedes aegypti mosquitoes. Biology Letters, 18(9), 20220270.

Bates, A. S., Schlegel, P., Roberts, R. J., Drummond, N., Tamimi, I. F., Turnbull, R., … & Jefferis, G. S. (2020). Complete connectomic reconstruction of olfactory projection neurons in the fly brain. Current Biology, 30(16), 3183-3199.

Chang, H., Cassau, S., Krieger, J., Guo, X., Knaden, M., Kang, L., & Hansson, B. S. (2023). A chemical defense deters cannibalism in migratory locusts. Science, 380(6644), 537-543.

Laurent, G. (2002). Olfactory network dynamics and the coding of multidimensional signals. Nature reviews neuroscience, 3(11), 884-895.

Nizampatnam, S., Saha, D., Chandak, R., & Raman, B. (2018). Dynamic contrast enhancement and flexible odor codes. Nature communications, 9(1), 3062.

Stopfer, M., Jayaraman, V., & Laurent, G. (2003). Intensity versus identity coding in an olfactory system. Neuron, 39(6), 991-1004.

Vinauger, C., Van Breugel, F., Locke, L. T., Tobin, K. K., Dickinson, M. H., Fairhall, A. L., … & Riffell, J. A. (2019). Visual-olfactory integration in the human disease vector mosquito Aedes aegypti. Current Biology, 29(15), 2509-2516.

Wei, J., Shao, W., Wang, X., Ge, J., Chen, X., Yu, D., & Kang, L. (2017). Composition and emission dynamics of migratory locust volatiles in response to changes in developmental stages and population density. Insect science, 24(1), 60-72.

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