Abstract
Animals typically avoid unwanted situations with stereotyped escape behavior. For instance, Drosophila larvae often escape from aversive stimuli to the head, such as mechanical stimuli and blue light irradiation, by backward locomotion. Responses to these aversive stimuli are mediated by a variety of sensory neurons including mechanosensory class III da (C3da) sensory neurons and blue-light responsive class IV da (C4da) sensory neurons and Bolwig's organ (BO). How these distinct sensory pathways evoke backward locomotion at the circuit level is still incompletely understood. Here we show that a pair of cholinergic neurons in the subesophageal zone, designated AMBs, evoke robust backward locomotion upon optogenetic activation. Anatomical and functional analysis shows that AMBs act upstream of MDNs, the command-like neurons for backward locomotion. Further functional analysis indicates that AMBs preferentially convey aversive blue light information from C4da neurons to MDNs to elicit backward locomotion, whereas aversive information from BO converges on MDNs through AMB-independent pathways. We also found that, unlike in adult flies, MDNs are dispensable for the dead end-evoked backward locomotion in larvae. Our findings thus reveal the neural circuits by which two distinct blue light-sensing pathways converge on the command-like neurons to evoke robust backward locomotion, and suggest that distinct but partially redundant neural circuits including the command-like neurons might be utilized to drive backward locomotion in response to different sensory stimuli as well as in adults and larvae.
Highlights
Dynamic locomotion with steering control is critical for animals to avoid unwanted situations [1,2,3]
Changes in movement direction are evoked by command neurons in the brain that function on local motor circuits to control direction and timing of muscle movements
A pair of ascending cholinergic neurons in subesophageal zone (SEZ) can trigger backward locomotion In order to systematically identify neurons involved in control of a specific type of escape behavior, backward locomotion, we conducted an optogenetic screen using the Janelia GAL4 collection together with UAS-CsChrimson [27,28]
Summary
Dynamic locomotion with steering control is critical for animals to avoid unwanted situations [1,2,3]. Animals generally walk forward but often switch to backward when sensing insurmountable obstacles or potentially dangerous stimuli in their path. Animals often have dedicated control systems for backward locomotion [4,5]. A recent study indicates that the TwoLumps ascending neurons mediate the touch-evoked backward walk through MDN activation in response to touch stimuli on the anterior legs [9]. MDNs function in Drosophila larvae as well as adults to evoke backward locomotion in response to mechanical stimuli on the head [7]. Structural and functional studies indicated that larval MDNs promote backward locomotion through activating the backward specific premotor neurons and simultaneously suppressing forward premotor neurons through distinct postsynaptic partners [7], though sensory control of the larval backward locomotion remains elusive
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