Cell
Volume 167, Issue 3, 20 October 2016, Pages 858-870.e19
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Article
Competitive Disinhibition Mediates Behavioral Choice and Sequences in Drosophila

https://doi.org/10.1016/j.cell.2016.09.009Get rights and content
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Highlights

  • Mechanical stimuli in Drosophila larvae evoke hunch, bend, or a sequence of the two

  • Reciprocally connected feedforward inhibitory interneurons mediate behavioral choice

  • Feedback disinhibition biases behavioral choice and prevents sequence reversals

  • Lateral disinhibition promotes sequence transitions

Summary

Even a simple sensory stimulus can elicit distinct innate behaviors and sequences. During sensorimotor decisions, competitive interactions among neurons that promote distinct behaviors must ensure the selection and maintenance of one behavior, while suppressing others. The circuit implementation of these competitive interactions is still an open question. By combining comprehensive electron microscopy reconstruction of inhibitory interneuron networks, modeling, electrophysiology, and behavioral studies, we determined the circuit mechanisms that contribute to the Drosophila larval sensorimotor decision to startle, explore, or perform a sequence of the two in response to a mechanosensory stimulus. Together, these studies reveal that, early in sensory processing, (1) reciprocally connected feedforward inhibitory interneurons implement behavioral choice, (2) local feedback disinhibition provides positive feedback that consolidates and maintains the chosen behavior, and (3) lateral disinhibition promotes sequence transitions. The combination of these interconnected circuit motifs can implement both behavior selection and the serial organization of behaviors into a sequence.

Keywords

behavioral choice
behavioral sequences
disinihibition
recurrent inhibition
Drosophila
sensory processing
EM connectome

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