A pair of ascending neurons in the subesophageal zone mediates aversive sensory inputs-evoked backward locomotion in Drosophila larvae

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.

Two Parallel Pathways Mediate Olfactory-Driven Backward Locomotion

“…In addition, we identify the SEZ as participating in MDN input (Figure 3A, C) and surprisingly in olfactory MDN input (Figure 7C). Our results combined with recent results in larvae 59 suggest that SEZ neurons also act as modality integrators responding at least to olfactory and visual inputs although it still remains to be examined whether AMBs and MooSEZs are identical neurons and whether the adult MooSEZs also respond to light. In this context it seems that the mechanosensory input from the VNC bypasses the SEZ and projects directly to the region where MDN dendrites arborize 20 .…”

“…Behavior analysis of these larvae revealed that the backward crawling was maintained. A recent study in larvae reported the existence of two SEZ neurons, AMB neurons, which mediate backward crawling via activation of MDNs 59 . In contrast, MooSEZs seem to be able to act in an MDN-independent manner.…”

Two Parallel Pathways Mediate Olfactory-Driven Backward Locomotion

“…The anatomy of the MooSEZ suggests dendritic regions mostly in the ventral SEZ, and putative presynaptic projections in the inferior protocerebrum. A neuron with similar behavior and morphology in larvae expresses pre-and postsynaptic markers in the respective regions (AMB 59 ), supporting this notion. In adults, the protocerebral innervation is in the lower LAL, posterior to the AL, possibly reaching into the wedge, lateroventral to the AL.…”

“…Behavior analysis of these larvae revealed that the backward crawling was maintained ( Figure S7B and Movie S8). A recent study in larvae reported the existence of two SEZ neurons, AMB neurons, which mediate backward crawling via activation of MDNs 59 . In contrast, MooSEZs seem to be able to act also in an MDNindependent manner.…”

Neural Design Principles for Subjective Experience: Implications for Insects

“…Optogenetic regulation of these interneurons can either induce or reduce rolling behavior ( Yoshino et al, 2017 ). While these segmental nociceptive escape circuits are sufficient to drive motor behaviors, the ascending interneuron projections enable coordination between segmental levels and lead to activation of brain interneurons (see section “Nociceptive Processing Pathways in the Drosophila Larval Brain”) that can modulate behaviors via descending pathways ( Figure 3B ; Ohyama et al, 2015 ; Kaneko et al, 2017 ; Yoshino et al, 2017 ; Burgos et al, 2018 ; Carreira-Rosario et al, 2018 ; Hu et al, 2018 ; Omamiuda-Ishikawa et al, 2020 ).…”