Neuronal control of locomotor handedness in Drosophila
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Abstract
Genetically identical individuals display variability in their physiology, morphology, and behaviors, even when reared in essentially identical environments, but there is little mechanistic understanding of the basis of such variation. Here, we investigated whether Drosophila melanogaster displays individual-to-individual variation in locomotor behaviors. We developed a new high-throughout platform capable of measuring the exploratory behavior of hundreds of individual flies simultaneously. With this approach, we find that, during exploratory walking, individual flies exhibit significant bias in their left vs. right locomotor choices, with some flies being strongly left biased or right biased. This idiosyncrasy was present in all genotypes examined, including wild-derived populations and inbred isogenic laboratory strains. The biases of individual flies persist for their lifetime and are nonheritable: i.e., mating two left-biased individuals does not yield left-biased progeny. This locomotor handedness is uncorrelated with other asymmetries, such as the handedness of gut twisting, leg-length asymmetry, and wing-folding preference. Using transgenics and mutants, we find that the magnitude of locomotor handedness is under the control of columnar neurons within the central complex, a brain region implicated in motor planning and execution. When these neurons are silenced, exploratory laterality increases, with more extreme leftiness and rightiness. This observation intriguingly implies that the brain may be able to dynamically regulate behavioral individuality.
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Our results provide insight into mechanisms underlying individual differences in navigation behavior.
“Our results also provide insight into mechanisms underlying individual differences in navigation behavior53,54.”
From Multimodal cue integration and learning in a neural representation of head direction (2025) · cites this paper as [54]
Cites
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“Furthermore, a genome-wide association study in a panel of inbred lines implicated SNPs within Ten-a as affecting variability in locomotor handedness (22).”
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Hulse, B. K., Haberkern, H., Franconville, R., Turner-Evans, D., Takemura, S.-Y., Wolff, T., Noorman, M., Dreher, M., Dan, C., Parekh, R., et al. (2021) · eLife · doi:10.7554/elife.66039 · Cited by 392 · see citing works
Behavioral idiosyncrasy reveals genetic control of phenotypic variability
Ayroles, J. F., Buchanan, S. M., O’Leary, C., Skutt-Kakaria, K., Grenier, J. K., Clark, A. G., Hartl, D. L., & de Bivort, B. L. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1503830112 · Cited by 218 · see citing works
“, a young adult with a strong left bias will display this bias throughout its life) (18).”
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Multimodal cue integration and learning in a neural representation of head direction
Basnak, M. A., Kutschireiter, A., Okubo, T. S., Chen, A., Gorelik, P., Drugowitsch, J., & Wilson, R. I. (2025) · Nature Neuroscience · doi:10.1038/s41593-024-01823-z · Cited by 13 · see citing works
- Authors
- Buchanan, S. M., Kain, J. S., & de Bivort, B. L.
- Affiliations
- Harvard University (US)
- The Rowland Institute at Harvard, Cambridge, MA 02142; and
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2015-05-07
- Volume
- 112
- Issue
- 21
- Pages
- 6700-6705
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC4450378
- OpenAlex
- W1539597651
- Cited by
- 179
- References
- 4
- Citations by year
- 2026: 20 · 2025: 22 · 2024: 24 · 2023: 15 · 2022: 17 · 2021: 20 · 2020: 17 · 2019: 10 · 2018: 13 · 2017: 12 · 2016: 4 · 2015: 4
- FWCI
- 6.61
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Licence
- cc-by
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- arXiv (Cornell University) (submittedVersion)
- arXiv (Cornell University) (cc-by)
- Funders
- Rowland Institute at Harvard
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Hemispheric Asymmetry in Neuroscience
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Keywords
- Drosophila melanogaster, exploratory behavior, laterality, central complex, leg length asymmetry
- MeSH terms
- Animals, Behavior, Animal, Brain, Drosophila melanogaster, Exploratory Behavior, Female, Functional Laterality, Locomotion, Male, Models, Neurological, Genes, Insect, Animals, Genetically Modified
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