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Neuron. 2017 Aug 2;95(3):623-638.e4. doi: 10.1016/j.neuron.2017.06.034. Epub 2017 Jul 14.

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

Author information

1
Life Sciences Institute and Department of Cell and Developmental Biology, University of Michigan, Ann Arbor, MI 48109, USA.
2
Life Sciences Institute and Department of Cell and Developmental Biology, University of Michigan, Ann Arbor, MI 48109, USA; Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI 48109, USA.
3
Department of Computer Science, Northern Illinois University, DeKalb, IL 60115, USA.
4
Department of Neurobiology, Duke University Medical School, Durham, NC 27710, USA.
5
Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI 48109, USA.
6
Life Sciences Institute and Department of Cell and Developmental Biology, University of Michigan, Ann Arbor, MI 48109, USA. Electronic address: bingye@umich.edu.

Abstract

How experiences during development cause long-lasting changes in sensory circuits and affect behavior in mature animals are poorly understood. Here we establish a novel system for mechanistic analysis of the plasticity of developing neural circuits by showing that sensory experience during development alters nociceptive behavior and circuit physiology in Drosophila larvae. Despite the convergence of nociceptive and mechanosensory inputs on common second-order neurons (SONs), developmental noxious input modifies transmission from nociceptors to their SONs, but not from mechanosensors to the same SONs, which suggests striking sensory pathway specificity. These SONs activate serotonergic neurons to inhibit nociceptor-to-SON transmission; stimulation of nociceptors during development sensitizes nociceptor presynapses to this feedback inhibition. Our results demonstrate that, unlike associative learning, which involves inputs from two sensory pathways, sensory pathway-specific plasticity in the Drosophila nociceptive circuit is in part established through feedback modulation. This study elucidates a novel mechanism that enables pathway-specific plasticity in sensory systems. VIDEO ABSTRACT.

KEYWORDS:

Drosophila; development; neural circuit; nociceptive behavior; nociceptive circuit; pathway-specific; plasticity; presynaptic inhibition; sensory system; serotonin

PMID:
28712652
PMCID:
PMC5555049
DOI:
10.1016/j.neuron.2017.06.034
[Indexed for MEDLINE]
Free PMC Article

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