TwoLumps Ascending Neurons Mediate Touch-Evoked Reversal of Walking Direction in Drosophila

Sen, Rajyashree; Wang, Kaiyu; Dickson, Barry J.

doi:10.1016/j.cub.2019.11.004

Cited by 18 publications

(44 citation statements)

References 28 publications

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“…Before embarking on a detailed investigation of how MDN couples to leg motor circuits, we first sought to better understand the impact of MDN activation on leg movements. Previous studies of MDN-triggered backward walking have examined only the translocation of the body [10][11][12] or the pattern of footfalls 10 . It remains to be determined how MDN alters leg joint kinematics, a more direct and higher-dimensional readout of motor circuit activity.…”

Section: Joint Kinematics Suggest That Hindlegs Dominate Mdn-triggerementioning

confidence: 99%

“…In behavioral assays, the fly typically backs up for several steps when it encounters an obstacle, despite receiving only a transient mechanosensory stimulus. However, upon artificial activation of MDNs, the fly walks backwards only so long as the stimulus persists 10,11 . These results suggest that circuits in the brain convert an acute mechanosensory stimulus into tonic activation of MDNs.…”

Section: Stance Phasementioning

confidence: 99%

“…Flies with genetically silenced MDNs are unable to walk backwards when they encounter a physical obstacle, whereas freely roaming flies walk backwards if the MDNs are artificially activated 10 . MDNs receive input from neurons conveying mechanosensory cues 11 (representing a possible obstacle) and from visual neurons that detect a looming stimulus 12 (a potential threat). The MDNs are also present in larvae, where they mediate backward crawling 13 .…”

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confidence: 99%

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Distributed control of motor circuits for backward walking inDrosophila

Feng

Sen

Minegishi

et al. 2020

Preprint

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How do descending inputs from the brain control leg motor circuits to change the way an animal walks? Conceptually, descending neurons are thought to function either as command-type neurons, in which a single type of descending neuron exerts a high-level control to elicit a coordinated change in motor output, or through a more distributed population coding mechanism, whereby a group of neurons, each with local effects, act in combination to elicit a global motor response. The Drosophila Moonwalker Descending Neurons (MDNs), which alter leg motor circuit dynamics so that the fly walks backwards, exemplify the command-type mechanism. Here, we identify several dozen MDN target neurons within the leg motor circuits, and show that two of them mediate distinct and highly-specific changes in leg muscle activity during backward walking: LIN156 neurons provide the hindleg power stroke during stance phase; LIN128 neurons lift the legs at the end of stance to initiate swing. Through these two effector neurons, MDN directly controls both the stance and swing phases of the backward stepping cycle. MDN exerts these changes only upon the hindlegs; the fore- and midlegs follow passively through ground contact. These findings suggest that command-type descending neurons can also operate through the distributed control of local motor circuits.

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Section: Joint Kinematics Suggest That Hindlegs Dominate Mdn-triggerementioning

confidence: 99%

Section: Stance Phasementioning

confidence: 99%

mentioning

confidence: 99%

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Distributed control of motor circuits for backward walking inDrosophila

Feng

Sen

Minegishi

et al. 2020

Preprint

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“…MDNs are required to walk back from dead ends [ 6 ] and to walk away from visual threat [ 8 ]. 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 also function in Drosophila larvae as well as adults to evoke backward locomotion in response to mechanical stimuli on the head [ 7 ].…”

Section: Introductionmentioning

confidence: 99%

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

2020

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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.

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“…Genetic combinatorial methods typically use either the regulatory elements of two neurally-expressed genes or exploit stochastic events to limit transgene targeting to a subpopulation of a larger group of neurons. In fruit flies, both types of method have been used to target single cells under optimal conditions (Aso et al, 2014;Gao et al, 2008;Gordon and Scott, 2009;Kohatsu et al, 2011;Lee and Luo, 1999;Luan et al, 2012;Pool et al, 2014;Sen et al, 2019;Shang et al, 2008;Yu et al, 2010), and combinatorial approaches using three regulatory elements have achieved some success (Dolan et al, 2017;Pankova and Borst, 2017;Shirangi et al, 2016;Sullivan et al, 2019). However, general limitations apply to all such approaches: stochastic methods are, by nature, poorly reproducible, while combinatorial methods are labor-intensive, often requiring the characterization of many neurally active enhancer elements (Dionne et al, 2018;Tirian et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

Cre-assisted fine-mapping of neural circuits using orthogonal split inteins

Luan

Kuzin

Odenwald

et al. 2020

eLife

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Existing genetic methods of neuronal targeting do not routinely achieve the resolution required for mapping brain circuits. New approaches are thus necessary. Here, we introduce a method for refined neuronal targeting that can be applied iteratively. Restriction achieved at the first step can be further refined in a second step, if necessary. The method relies on first isolating neurons within a targeted group (i.e. Gal4 pattern) according to their developmental lineages, and then intersectionally limiting the number of lineages by selecting only those in which two distinct neuroblast enhancers are active. The neuroblast enhancers drive expression of split Cre recombinase fragments. These are fused to non-interacting pairs of split inteins, which ensure reconstitution of active Cre when all fragments are expressed in the same neuroblast. Active Cre renders all neuroblast-derived cells in a lineage permissive for Gal4 activity. We demonstrate how this system can facilitate neural circuit-mapping in Drosophila.

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TwoLumps Ascending Neurons Mediate Touch-Evoked Reversal of Walking Direction in Drosophila

Abstract: Highlights d TwoLumps Ascending (TLA) neurons are required for backward locomotion d TLAs trigger backward locomotion via the Moonwalker Descending Neurons (MDNs) d TLAs provide feedforward input to MDNs d TLAs mediate touch-evoked backing up

Cited by 18 publications

References 28 publications

Distributed control of motor circuits for backward walking inDrosophila

Distributed control of motor circuits for backward walking inDrosophila

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

Cre-assisted fine-mapping of neural circuits using orthogonal split inteins

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