Olfactory stimuli and moonwalker SEZ neurons can drive backward locomotion in Drosophila

• Published in: Current biology 2022-03, Vol.32 (5), p.1131-1149.e7
• Main Authors: Israel, Shai, Rozenfeld, Eyal, Weber, Denise, Huetteroth, Wolf, Parnas, Moshe
• Format: Article
• Language: English
• Subjects: Animals; backward locomotion; Brain - physiology; descending neurons; Drosophila; Drosophila - physiology; Drosophila melanogaster - physiology; Locomotion - physiology; MDNs; MooSEZs; motor control; neural pathways; Neurons - physiology; olfaction; sensorimotor integration; SEZ
• ISSN: 0960-9822; 1879-0445; 1879-0445
• DOI: 10.1016/j.cub.2022.01.035

How different sensory stimuli are collected, processed, and further transformed into a coordinated motor response is a fundamental question in neuroscience. In particular, the internal and external conditions that drive animals to switch to backward walking and the mechanisms by which the nervous system supports such behavior are still unknown. In fruit flies, moonwalker descending neurons (MDNs) are considered command-type neurons for backward locomotion as they receive visual and mechanosensory inputs and transmit motor-related signals to downstream neurons to elicit backward locomotion. Whether other modalities converge onto MDNs, which central brain neurons activate MDNs, and whether other retreat-driving pathways exist is currently unknown. Here, we show that olfactory stimulation can elicit MDN-mediated backward locomotion. Moreover, we identify the moonwalker subesophageal zone neurons (MooSEZs), a pair of bilateral neurons, which can trigger straight and rotational backward locomotion. MooSEZs act via postsynaptic MDNs and via other descending neurons. Although they respond to olfactory input, they are not required for odor-induced backward walking. Thus, this work reveals an important modality input to MDNs, a novel set of neurons presynaptic to MDNs driving backward locomotion and an MDN-independent backward locomotion pathway. [Display omitted] •MooSEZs elicit backward locomotion via MDN-dependent and MDN-independent pathways•MooSEZs are connected to MDNs and other descending neurons•MooSEZs and MDNs both respond to olfactory input•MooSEZs can trigger rotational backward locomotion Israel et al. describe olfactory-driven backward locomotion that is mediated by MDNs. They also identify a pair of bilateral central brain neurons, MooSEZs, which respond to odor input and contribute to rotational backward locomotion via postsynaptic MDNs and additional descending neurons.