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Asymmetric activity of NetrinB controls laterality of the Drosophila brain

Author

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  • F. Lapraz

    (Université Côte d’Azur, CNRS, Inserm, iBV)

  • C. Boutres

    (Université Côte d’Azur, CNRS, Inserm, iBV)

  • C. Fixary-Schuster

    (Université Côte d’Azur, CNRS, Inserm, iBV)

  • B. R. Queiroz

    (Université Côte d’Azur, CNRS, Inserm, iBV)

  • P. Y. Plaçais

    (PSL Research University)

  • D. Cerezo

    (Université Côte d’Azur, CNRS, Inserm, iBV)

  • F. Besse

    (Université Côte d’Azur, CNRS, Inserm, iBV)

  • T. Préat

    (PSL Research University)

  • S. Noselli

    (Université Côte d’Azur, CNRS, Inserm, iBV)

Abstract

Left-Right (LR) asymmetry of the nervous system is widespread across animals and is thought to be important for cognition and behaviour. But in contrast to visceral organ asymmetry, the genetic basis and function of brain laterality remain only poorly characterized. In this study, we performed RNAi screening to identify genes controlling brain asymmetry in Drosophila. We found that the conserved NetrinB (NetB) pathway is required for a small group of bilateral neurons to project asymmetrically into a pair of neuropils (Asymmetrical Bodies, AB) in the central brain in both sexes. While neurons project unilaterally into the right AB in wild-type flies, netB mutants show a bilateral projection phenotype and hence lose asymmetry. Developmental time course analysis reveals an initially bilateral connectivity, eventually resolving into a right asymmetrical circuit during metamorphosis, with the NetB pathway being required just prior symmetry breaking. We show using unilateral clonal analysis that netB activity is required specifically on the right side for neurons to innervate the right AB. We finally show that loss of NetB pathway activity leads to specific alteration of long-term memory, providing a functional link between asymmetrical circuitry determined by NetB and animal cognitive functions.

Suggested Citation

  • F. Lapraz & C. Boutres & C. Fixary-Schuster & B. R. Queiroz & P. Y. Plaçais & D. Cerezo & F. Besse & T. Préat & S. Noselli, 2023. "Asymmetric activity of NetrinB controls laterality of the Drosophila brain," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36644-4
    DOI: 10.1038/s41467-023-36644-4
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    References listed on IDEAS

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    1. Shunya Hozumi & Reo Maeda & Kiichiro Taniguchi & Maiko Kanai & Syuichi Shirakabe & Takeshi Sasamura & Pauline Spéder & Stéphane Noselli & Toshiro Aigaki & Ryutaro Murakami & Kenji Matsuno, 2006. "An unconventional myosin in Drosophila reverses the default handedness in visceral organs," Nature, Nature, vol. 440(7085), pages 798-802, April.
    2. Alberto Pascual & Kai-Lian Huang & Julie Neveu & Thomas Préat, 2004. "Brain asymmetry and long-term memory," Nature, Nature, vol. 427(6975), pages 605-606, February.
    3. Pauline Spéder & Géza Ádám & Stéphane Noselli, 2006. "Type ID unconventional myosin controls left–right asymmetry in Drosophila," Nature, Nature, vol. 440(7085), pages 803-807, April.
    4. Chloé Dominici & Juan Antonio Moreno-Bravo & Sergi Roig Puiggros & Quentin Rappeneau & Nicolas Rama & Pauline Vieugue & Agns Bernet & Patrick Mehlen & Alain Chédotal, 2017. "Floor-plate-derived netrin-1 is dispensable for commissural axon guidance," Nature, Nature, vol. 545(7654), pages 350-354, May.
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