IDEAS home Printed from https://ideas.repec.org/a/plo/pone00/0000443.html
   My bibliography  Save this article

Order in Spontaneous Behavior

Author

Listed:
  • Alexander Maye
  • Chih-hao Hsieh
  • George Sugihara
  • Björn Brembs

Abstract

Brains are usually described as input/output systems: they transform sensory input into motor output. However, the motor output of brains (behavior) is notoriously variable, even under identical sensory conditions. The question of whether this behavioral variability merely reflects residual deviations due to extrinsic random noise in such otherwise deterministic systems or an intrinsic, adaptive indeterminacy trait is central for the basic understanding of brain function. Instead of random noise, we find a fractal order (resembling Lévy flights) in the temporal structure of spontaneous flight maneuvers in tethered Drosophila fruit flies. Lévy-like probabilistic behavior patterns are evolutionarily conserved, suggesting a general neural mechanism underlying spontaneous behavior. Drosophila can produce these patterns endogenously, without any external cues. The fly's behavior is controlled by brain circuits which operate as a nonlinear system with unstable dynamics far from equilibrium. These findings suggest that both general models of brain function and autonomous agents ought to include biologically relevant nonlinear, endogenous behavior-initiating mechanisms if they strive to realistically simulate biological brains or out-compete other agents.

Suggested Citation

  • Alexander Maye & Chih-hao Hsieh & George Sugihara & Björn Brembs, 2007. "Order in Spontaneous Behavior," PLOS ONE, Public Library of Science, vol. 2(5), pages 1-14, May.
    • Handle: RePEc:plo:pone00:0000443
    DOI: 10.1371/journal.pone.0000443
    as

    Download full text from publisher

    File URL: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0000443
    Download Restriction: no
    File URL: https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0000443&type=printable
    Download Restriction: no
    File URL: https://libkey.io/10.1371/journal.pone.0000443?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. G. M. Viswanathan & Sergey V. Buldyrev & Shlomo Havlin & M. G. E. da Luz & E. P. Raposo & H. Eugene Stanley, 1999. "Optimizing the success of random searches," Nature, Nature, vol. 401(6756), pages 911-914, October.
    2. João Gama Oliveira & Albert-László Barabási, 2005. "Darwin and Einstein correspondence patterns," Nature, Nature, vol. 437(7063), pages 1251-1251, October.
    3. Geoffrey F. Miller, "undated". "Protean Primates: The Evolution of Adaptive Unpredictability in Competition and Courtship," ELSE working papers 046, ESRC Centre on Economics Learning and Social Evolution.
    4. Gianpietro Malescio, 2005. "Predicting with unpredictability," Nature, Nature, vol. 434(7037), pages 1073-1073, April.
    5. Leslie C. Osborne & Stephen G. Lisberger & William Bialek, 2005. "A sensory source for motor variation," Nature, Nature, vol. 437(7057), pages 412-416, September.
    6. Barbara Webb, 2002. "Robots in invertebrate neuroscience," Nature, Nature, vol. 417(6886), pages 359-363, May.
    7. Chih-hao Hsieh & Sarah M. Glaser & Andrew J. Lucas & George Sugihara, 2005. "Distinguishing random environmental fluctuations from ecological catastrophes for the North Pacific Ocean," Nature, Nature, vol. 435(7040), pages 336-340, May.
    8. D. Brockmann & L. Hufnagel & T. Geisel, 2006. "The scaling laws of human travel," Nature, Nature, vol. 439(7075), pages 462-465, January.
    9. Peter Ashwin & Marc Timme, 2005. "When instability makes sense," Nature, Nature, vol. 436(7047), pages 36-37, July.
    10. Shu-Ju Tu & Ephraim Fischbach, 2005. "A Study On The Randomness Of The Digits Of Π," International Journal of Modern Physics C (IJMPC), World Scientific Publishing Co. Pte. Ltd., vol. 16(02), pages 281-294.
    11. Alison Abbott, 2007. "Working out the bugs," Nature, Nature, vol. 445(7125), pages 250-253, January.
    12. Albert-László Barabási, 2005. "The origin of bursts and heavy tails in human dynamics," Nature, Nature, vol. 435(7039), pages 207-211, May.
    13. Evelyn Fox Keller, 2007. "A clash of two cultures," Nature, Nature, vol. 445(7128), pages 603-603, February.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Taro Ueno & Naoki Masuda & Shoen Kume & Kazuhiko Kume, 2012. "Dopamine Modulates the Rest Period Length without Perturbation of Its Power Law Distribution in Drosophila melanogaster," PLOS ONE, Public Library of Science, vol. 7(2), pages 1-12, February.
    2. Surya G Nurzaman & Yoshio Matsumoto & Yutaka Nakamura & Kazumichi Shirai & Satoshi Koizumi & Hiroshi Ishiguro, 2011. "From Lévy to Brownian: A Computational Model Based on Biological Fluctuation," PLOS ONE, Public Library of Science, vol. 6(2), pages 1-11, February.
    3. Andrea Censi & Andrew D Straw & Rosalyn W Sayaman & Richard M Murray & Michael H Dickinson, 2013. "Discriminating External and Internal Causes for Heading Changes in Freely Flying Drosophila," PLOS Computational Biology, Public Library of Science, vol. 9(2), pages 1-14, February.
    4. Sepideh Bazazi & Frederic Bartumeus & Joseph J Hale & Iain D Couzin, 2012. "Intermittent Motion in Desert Locusts: Behavioural Complexity in Simple Environments," PLOS Computational Biology, Public Library of Science, vol. 8(5), pages 1-10, May.
    5. Kin Fai Ellick Wong & Cecilia Cheng, 2013. "Predictable or Not? Individuals’ Risk Decisions Do Not Necessarily Predict Their Next Ones," PLOS ONE, Public Library of Science, vol. 8(2), pages 1-5, February.
    6. Masato S Abe & Masakazu Shimada, 2015. "Lévy Walks Suboptimal under Predation Risk," PLOS Computational Biology, Public Library of Science, vol. 11(11), pages 1-16, November.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Fan, Chao & Guo, Jin-Li & Zha, Yi-Long, 2012. "Fractal analysis on human dynamics of library loans," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 391(24), pages 6617-6625.
    2. Wang, Yanjun & Zhang, Qiqian & Zhu, Chenping & Hu, Minghua & Duong, Vu, 2016. "Human activity under high pressure: A case study on fluctuation scaling of air traffic controller’s communication behaviors," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 441(C), pages 151-157.
    3. Li, Zhenpeng & Tang, Xijin & Zhou, Haijun & Yan, Donghui, 2018. "An empirical investigation and theoretic modeling for the collective online visiting behaviors," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 503(C), pages 969-980.
    4. Ferreira, A.S. & Raposo, E.P. & Viswanathan, G.M. & da Luz, M.G.E., 2012. "The influence of the environment on Lévy random search efficiency: Fractality and memory effects," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 391(11), pages 3234-3246.
    5. Chen, Ning & Zhu, Xuzhen & Chen, Yanyan, 2019. "Information spreading on complex networks with general group distribution," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 523(C), pages 671-676.
    6. Toru Nakamura & Toru Takumi & Atsuko Takano & Fumiyuki Hatanaka & Yoshiharu Yamamoto, 2013. "Characterization and Modeling of Intermittent Locomotor Dynamics in Clock Gene-Deficient Mice," PLOS ONE, Public Library of Science, vol. 8(3), pages 1-8, March.
    7. Qi, Jie & Rong, Zhihai, 2013. "The emergence of scaling laws search dynamics in a particle swarm optimization," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 392(6), pages 1522-1531.
    8. Qianqian Liu & Qun Wang, 2017. "A comparative study on uncooperative search models in survivor search and rescue," Natural Hazards: Journal of the International Society for the Prevention and Mitigation of Natural Hazards, Springer;International Society for the Prevention and Mitigation of Natural Hazards, vol. 89(2), pages 843-857, November.
    9. E P Raposo & F Bartumeus & M G E da Luz & P J Ribeiro-Neto & T A Souza & G M Viswanathan, 2011. "How Landscape Heterogeneity Frames Optimal Diffusivity in Searching Processes," PLOS Computational Biology, Public Library of Science, vol. 7(11), pages 1-8, November.
    10. Tomassini, Marco, 2016. "Lévy flights in neutral fitness landscapes," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 448(C), pages 163-171.
    11. Wang, Jian & Song, Weiguo & Zheng, Hongyang & Telesca, Luciano, 2010. "Temporal scaling behavior of human-caused fires and their connection to relative humidity of the atmosphere," Ecological Modelling, Elsevier, vol. 221(1), pages 85-89.
    12. Baronchelli, Andrea & Radicchi, Filippo, 2013. "Lévy flights in human behavior and cognition," Chaos, Solitons & Fractals, Elsevier, vol. 56(C), pages 101-105.
    13. Juan V Escobar & Didier Sornette, 2015. "Dynamical Signatures of Collective Quality Grading in a Social Activity: Attendance to Motion Pictures," PLOS ONE, Public Library of Science, vol. 10(1), pages 1-15, January.
    14. Sanja Šćepanović & Igor Mishkovski & Pan Hui & Jukka K Nurminen & Antti Ylä-Jääski, 2015. "Mobile Phone Call Data as a Regional Socio-Economic Proxy Indicator," PLOS ONE, Public Library of Science, vol. 10(4), pages 1-15, April.
    15. Ndibatya, Innocent & Booysen, M.J., 2021. "Characterizing the movement patterns of minibus taxis in Kampala's paratransit system," Journal of Transport Geography, Elsevier, vol. 92(C).
    16. Lin Li & Lei Yang & Haihong Zhu & Rongrong Dai, 2015. "Explorative Analysis of Wuhan Intra-Urban Human Mobility Using Social Media Check-In Data," PLOS ONE, Public Library of Science, vol. 10(8), pages 1-19, August.
    17. Xiang Liu & Feicheng Ma, 2013. "Transfer and distribution of knowledge creation activities of bio-scientists in knowledge space," Scientometrics, Springer;Akadémiai Kiadó, vol. 95(1), pages 299-310, April.
    18. Filippo Radicchi & Andrea Baronchelli & Luís A N Amaral, 2012. "Rationality, Irrationality and Escalating Behavior in Lowest Unique Bid Auctions," PLOS ONE, Public Library of Science, vol. 7(1), pages 1-8, January.
    19. Priscila C A da Silva & Tiago V Rosembach & Anésia A Santos & Márcio S Rocha & Marcelo L Martins, 2014. "Normal and Tumoral Melanocytes Exhibit q-Gaussian Random Search Patterns," PLOS ONE, Public Library of Science, vol. 9(9), pages 1-13, September.
    20. Moolenaar, Hanneke E. & Grasman, Johan & Selten, Frank M. & de Gee, Maarten, 2007. "Testing a method for analyzing the effect of parameter change in climate driven ecological systems," Ecological Modelling, Elsevier, vol. 205(3), pages 289-300.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:plo:pone00:0000443. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: plosone (email available below). General contact details of provider: https://journals.plos.org/plosone/ .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.