Serotonergic Modulation Enables Pathway-Specific Plasticity in a Developing Sensory Circuit in Drosophila

Kaneko, Takuya; Macara, Ann Marie; Li, Ruonan; Hu, Yujia; Iwasaki, Kenichi; Dunnings, Zane; Firestone, Ethan; Horvatic, Shawn; Guntur, Ananya; Shafer, Orie T.; Yang, Chung Hui; Zhou, Jie; Yan, Bing

doi:10.1016/j.neuron.2017.07.023

Cited by 21 publications

(18 citation statements)

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“…( Figure 7—figure supplement 1A–D ). We note that PMSIs also include A02a-j neurons ( Kaneko et al, 2017 ), so although our manipulations are not specific to A02e and A02g neurons, these results are consistent with PMSI neurons, perhaps including those downstream of DnBs, promoting robust nocifensive behavior.…”

Section: Resultssupporting

confidence: 70%

Nociceptive interneurons control modular motor pathways to promote escape behavior in Drosophila

Burgos

Honjo

Ohyama

et al. 2018

eLife

108

132

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Rapid and efficient escape behaviors in response to noxious sensory stimuli are essential for protection and survival. Yet, how noxious stimuli are transformed to coordinated escape behaviors remains poorly understood. In Drosophila larvae, noxious stimuli trigger sequential body bending and corkscrew-like rolling behavior. We identified a population of interneurons in the nerve cord of Drosophila, termed Down-and-Back (DnB) neurons, that are activated by noxious heat, promote nociceptive behavior, and are required for robust escape responses to noxious stimuli. Electron microscopic circuit reconstruction shows that DnBs are targets of nociceptive and mechanosensory neurons, are directly presynaptic to pre-motor circuits, and link indirectly to Goro rolling command-like neurons. DnB activation promotes activity in Goro neurons, and coincident inactivation of Goro neurons prevents the rolling sequence but leaves intact body bending motor responses. Thus, activity from nociceptors to DnB interneurons coordinates modular elements of nociceptive escape behavior.

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Section: Resultssupporting

confidence: 70%

Nociceptive interneurons control modular motor pathways to promote escape behavior in Drosophila

Burgos

Honjo

Ohyama

et al. 2018

eLife

108

132

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“…Optogenetic activation of cIV multidendritic neurons during development sensitizes these sensory neurons, resulting in larvae being less likely to curl and roll in response to subsequent optogenetic stimulation (19). We show that cIV multidendritic neurons synapse onto pr1 neurons and that activation of pr1 neurons reduces the likelihood of larvae curling and rolling in response to a thermal probe.…”

Section: Discussionmentioning

confidence: 82%

“…The cIV multidendritic neurons are known to synapse onto the ventral region of the ventral nerve cord (VNC) (19,(45)(46)(47). We next tested whether pr1 VNC neurons were required for the curling and rolling response by genetically separating pr1-GAL4 brain lobe expression from VNC expression by combining the VNC-specific GAL4 inhibitor tsh-GAL80 (48) with pr1-GAL4.…”

Section: Significancementioning

confidence: 99%

“…Optogenetic stimulation of cIV multidendritic neurons during development sensitizes cIV multidendritic neurons and makes larvae less likely to curl and roll in response to subsequent optogenetic stimulation (19). Given that pr1 neurons are downstream of cIV multidendritic neurons, we hypothesized that activation of pr1 neurons during development would also suppress the nociceptive-like escape response.…”

Section: Significancementioning

confidence: 99%

“…Silencing cIV multidendritic sensory neurons with tetanus toxin eliminates this nociceptive-like escape response (8), whereas optogenetic activation of these neurons induces the curling and rolling escape response (8,17,18). These sensory neurons also display experience-dependent plasticity, as prolonged optogenetic activation during development sensitizes these neurons, resulting in larvae that are less likely to roll in response to subsequent optogenetic stimulation (19).…”

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confidence: 99%

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Drosophila melanogaster foraging regulates a nociceptive-like escape behavior through a developmentally plastic sensory circuit

Dason

Cheung

Anreiter

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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Painful or threatening experiences trigger escape responses that are guided by nociceptive neuronal circuitry. Although some components of this circuitry are known and conserved across animals, how this circuitry is regulated at the genetic and developmental levels is mostly unknown. To escape noxious stimuli, such as parasitoid wasp attacks, Drosophila melanogaster larvae generate a curling and rolling response. Rover and sitter allelic variants of the Drosophila foraging (for) gene differ in parasitoid wasp susceptibility, suggesting a link between for and nociception. By optogenetically activating cells associated with each of for’s promoters (pr1–pr4), we show that pr1 cells regulate larval escape behavior. In accordance with rover and sitter differences in parasitoid wasp susceptibility, we found that rovers have higher pr1 expression and increased sensitivity to nociception relative to sitters. The for null mutants display impaired responses to thermal nociception, which are rescued by restoring for expression in pr1 cells. Conversely, knockdown of for in pr1 cells phenocopies the for null mutant. To gain insight into the circuitry underlying this response, we used an intersectional approach and activity-dependent GFP reconstitution across synaptic partners (GRASP) to show that pr1 cells in the ventral nerve cord (VNC) are required for the nociceptive response, and that multidendritic sensory nociceptive neurons synapse onto pr1 neurons in the VNC. Finally, we show that activation of the pr1 circuit during development suppresses the escape response. Our data demonstrate a role of for in larval nociceptive behavior. This function is specific to for pr1 neurons in the VNC, guiding a developmentally plastic escape response circuit.

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Piezo-like Gene Regulates Locomotion in Drosophila Larvae

Wang

Liu

et al. 2019

Cell Reports

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Serotonergic Modulation Enables Pathway-Specific Plasticity in a Developing Sensory Circuit in Drosophila

Cited by 21 publications

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Nociceptive interneurons control modular motor pathways to promote escape behavior in Drosophila

Nociceptive interneurons control modular motor pathways to promote escape behavior in Drosophila

Drosophila melanogaster foraging regulates a nociceptive-like escape behavior through a developmentally plastic sensory circuit

Piezo-like Gene Regulates Locomotion in Drosophila Larvae

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