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Threat gates visual aversion via theta activity in Tachykinergic neurons

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  • Masato Tsuji

    (The University of Tokyo)

  • Yuto Nishizuka

    (The University of Tokyo)

  • Kazuo Emoto

    (The University of Tokyo
    The University of Tokyo)

Abstract

Animals must adapt sensory responses to an ever-changing environment for survival. Such sensory modulation is especially critical in a threatening situation, in which animals often promote aversive responses to, among others, visual stimuli. Recently, threatened Drosophila has been shown to exhibit a defensive internal state. Whether and how threatened Drosophila promotes visual aversion, however, remains elusive. Here we report that mechanical threats to Drosophila transiently gate aversion from an otherwise neutral visual object. We further identified the neuropeptide tachykinin, and a single cluster of neurons expressing it (“Tk-GAL42 ∩ Vglut neurons”), that are responsible for gating visual aversion. Calcium imaging analysis revealed that mechanical threats are encoded in Tk-GAL42 ∩ Vglut neurons as elevated activity. Remarkably, we also discovered that a visual object is encoded in Tk-GAL42 ∩ Vglut neurons as θ oscillation, which is causally linked to visual aversion. Our data reveal how a single cluster of neurons adapt organismal sensory response to a threatening situation through a neuropeptide and a combination of rate/temporal coding schemes.

Suggested Citation

  • Masato Tsuji & Yuto Nishizuka & Kazuo Emoto, 2023. "Threat gates visual aversion via theta activity in Tachykinergic neurons," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39667-z
    DOI: 10.1038/s41467-023-39667-z
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    1. Mark Dombrovski & Martin Y. Peek & Jin-Yong Park & Andrea Vaccari & Marissa Sumathipala & Carmen Morrow & Patrick Breads & Arthur Zhao & Yerbol Z. Kurmangaliyev & Piero Sanfilippo & Aadil Rehan & Jaso, 2023. "Publisher Correction: Synaptic gradients transform object location to action," Nature, Nature, vol. 615(7954), pages 26-26, March.
    2. Mark Dombrovski & Martin Y. Peek & Jin-Yong Park & Andrea Vaccari & Marissa Sumathipala & Carmen Morrow & Patrick Breads & Arthur Zhao & Yerbol Z. Kurmangaliyev & Piero Sanfilippo & Aadil Rehan & Jaso, 2023. "Synaptic gradients transform object location to action," Nature, Nature, vol. 613(7944), pages 534-542, January.
    3. Guillaume Etter & Suzanne Veldt & Jisoo Choi & Sylvain Williams, 2023. "Optogenetic frequency scrambling of hippocampal theta oscillations dissociates working memory retrieval from hippocampal spatiotemporal codes," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    4. A. Florido & E. R. Velasco & C. M. Soto-Faguás & A. Gomez-Gomez & L. Perez-Caballero & P. Molina & R. Nadal & O. J. Pozo & C. A. Saura & R. Andero, 2021. "Sex differences in fear memory consolidation via Tac2 signaling in mice," Nature Communications, Nature, vol. 12(1), pages 1-19, December.
    5. Cyril Dejean & Julien Courtin & Nikolaos Karalis & Fabrice Chaudun & Hélène Wurtz & Thomas C. M. Bienvenu & Cyril Herry, 2016. "Prefrontal neuronal assemblies temporally control fear behaviour," Nature, Nature, vol. 535(7612), pages 420-424, July.
    6. Suzuko Yorozu & Allan Wong & Brian J. Fischer & Heiko Dankert & Maurice J. Kernan & Azusa Kamikouchi & Kei Ito & David J. Anderson, 2009. "Distinct sensory representations of wind and near-field sound in the Drosophila brain," Nature, Nature, vol. 458(7235), pages 201-205, March.
    7. Ralf D. Wimmer & L. Ian Schmitt & Thomas J. Davidson & Miho Nakajima & Karl Deisseroth & Michael M. Halassa, 2015. "Thalamic control of sensory selection in divided attention," Nature, Nature, vol. 526(7575), pages 705-709, October.
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