The Function and Organization of the Motor System Controlling Flight Maneuvers in Flies

Lindsay, Theodore H.; Sustar, Anne; Dickinson, Michael H.

doi:10.1016/j.cub.2016.12.018

Cited by 98 publications

(149 citation statements)

References 55 publications

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“…Our data are consistent with a simple summation of the signals of the optomotor and the AX pathway. A recent study of the steering motor system indicates that direct flight muscles are divided into two groups: tonic muscles that are responsible for maintaining the trim of the flight motor and phasic muscles that are primarily recruited during the largest spontaneous turns [19]. We thus predict that the AX neuron makes particularly strong connections with phasic muscle motor neurons.…”

Section: Discussionmentioning

confidence: 92%

A Descending Neuron Correlated with the Rapid Steering Maneuvers of Flying Drosophila

2017

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Summary To navigate through the world, animals must stabilize their path against disturbances and change direction to avoid obstacles and to search for resources [1,2]. Locomotion is thus guided by sensory cues, but also depends on intrinsic processes, such as motivation and physiological state. Flies, for example, turn with the direction of large-field rotatory motion, an optomotor reflex that is thought to help them fly straight [3-5]. Occasionally, however, they execute fast turns, called body saccades, either spontaneously or in response to patterns of visual motion such as expansion [6-8]. These turns can be measured in tethered flying Drosophila [3,4,9], which facilitates the study of underlying neural mechanisms. Whereas there is evidence for an efference copy input to visual interneurons during saccades [10], the circuits that control spontaneous and visually elicited saccades are not well known. Using 2-photon calcium imaging and electrophysiological recordings in tethered flying Drosophila, we have identified a descending neuron whose activity is correlated with both spontaneous and visually elicited turns during tethered flight. The cell's activity in open- and closed-loop experiments suggests that it does not underlie slower compensatory responses to horizontal motion, but rather controls rapid changes in flight path. The activity of this neuron can explain some of the behavioral variability observed in response to visual motion and appears sufficient for eliciting turns when artificially activated. This work provides an entry point into studying the circuits underlying the control of rapid steering maneuvers in the fly brain.

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Section: Discussionmentioning

confidence: 92%

A Descending Neuron Correlated with the Rapid Steering Maneuvers of Flying Drosophila

2017

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“…In addition to the motion of internal sclerites, these techniques also allow visualization of the direct steering muscles during flight (Walker et al, 2014). In parallel, recent breakthroughs in Drosophila genetics also show great promise in revealing the role of specific direct steering muscles both individually and in combination with other muscles in different behaviors (Shirangi et al, 2013;Lindsay et al, 2017).…”

Section: The Wing Hinge Translates Muscle Contraction Into Wing Motionmentioning

confidence: 98%

“…Recent work on Drosophila using genetically encoded calcium reporters (GCaMP6f) in active muscles has revealed some very interesting aspects about the organization of steering muscles at the base of the wing hinge sclerites. The steering muscles in Drosophila are organized into two groups that are anatomically and functionally separated into the larger phasically activated muscles that control the major alteration in wing motion during distinct maneuvers, and the smaller tonic muscles that control the subtler modulations of wing motion (Lindsay et al, 2017). The transmission of strain from the indirect flight muscles, via hinge sclerites to the wings, may be described using a four-bar linkage model which includes the parascutal shelf, Ax1, Ax2 and the wing vein (e.g.…”

Section: The Wing Hinge Translates Muscle Contraction Into Wing Motionmentioning

confidence: 99%

Mechanics of the thorax in flies

Deora

Gundiah

Sane

2017

Journal of Experimental Biology

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Insects represent more than 60% of all multicellular life forms, and are easily among the most diverse and abundant organisms on earth. They evolved functional wings and the ability to fly, which enabled them to occupy diverse niches. Insects of the hyper-diverse orders show extreme miniaturization of their body size. The reduced body size, however, imposes steep constraints on flight ability, as their wings must flap faster to generate sufficient forces to stay aloft. Here, we discuss the various physiological and biomechanical adaptations of the thorax in flies which enabled them to overcome the myriad constraints of small body size, while ensuring very precise control of their wing motion. One such adaptation is the evolution of specialized myogenic or asynchronous muscles that power the high-frequency wing motion, in combination with neurogenic or synchronous steering muscles that control higher-order wing kinematic patterns. Additionally, passive cuticular linkages within the thorax coordinate fast and yet precise bilateral wing movement, in combination with an actively controlled clutch and gear system that enables flexible flight patterns. Thus, the study of thoracic biomechanics, along with the underlying sensory-motor processing, is central in understanding how the insect body form is adapted for flight.

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“…We used wide-field fluorescence imaging of muscle calcium signals with GCamp6f (Chen et al, 2013;Lindsay et al, 2017) to map the spatial organization of motor units in the fly femur during spontaneous tibia movements (Figures 1C and S1; Movie S1). We observed that spatial patterns of calcium activity were different for different movements (e.g., tibia flexion vs. extension).…”

Section: Organization and Recruitment Of Motor Units Controlling The mentioning

confidence: 99%

A size principle for leg motor control inDrosophila

Azevedo

Dickinson

Gurung

et al. 2019

Preprint

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To move the body, the brain must precisely coordinate patterns of activity among diverse populations of motor neurons. In many species, including vertebrates, the motor neurons innervating a given muscle fire in a specific order that is determined by a gradient of cellular size and electrical excitability. This hierarchy allows premotor circuits to recruit motor neurons of increasing force capacity in a task-dependent manner. However, it remains unclear whether such a size principle also applies to species with more compact motor systems, such as the fruit fly, Drosophila melanogaster, which has just 53 motor neurons per leg. Using in vivo calcium imaging and electrophysiology, we found that genetically-identified motor neurons controlling flexion of the fly tibia exhibit a gradient of anatomical, physiological, and functional properties consistent with the size principle. Large, fast motor neurons control high force, ballistic movements while small, slow motor neurons control low force, postural movements. Intermediate neurons fall between these two extremes. In behaving flies, motor neurons are recruited in order from slow to fast. This hierarchical organization suggests that slow and fast motor neurons control distinct motor regimes. Indeed, we find that optogenetic manipulation of each motor neuron type has distinct effects on the behavior of walking flies.

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The Function and Organization of the Motor System Controlling Flight Maneuvers in Flies

Cited by 98 publications

References 55 publications

A Descending Neuron Correlated with the Rapid Steering Maneuvers of Flying Drosophila

A Descending Neuron Correlated with the Rapid Steering Maneuvers of Flying Drosophila

Mechanics of the thorax in flies

A size principle for leg motor control inDrosophila

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