Neuromuscular embodiment of feedback control elements in
            <i>Drosophila</i>
            flight

Whitehead, Samuel C.; Leone, Sofia; Lindsay, Theodore H.; Meiselman, Matthew R.; Cowan, Noah J.; Dickinson, Michael H.; Yapici, Nilay; Stern, David L.; Shirangi, Troy R.; Cohen, Itai

doi:10.1126/sciadv.abo7461

Cited by 8 publications

(25 citation statements)

References 71 publications

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“…3, fourth column). In total, Drosophila is equipped with 12 flight steering muscles each of which likely contributes to a distinct function in flight control (Whitehead et al, 2022). The activation patterns of four of these muscles have been analyzed in response to optomotor stimulation during flight (first and second basalar muscles b1 and b2, as well as first pterale I muscle (i1) and the third pterale II muscle (iii1) (Heide and Götz, 1996; Dickinson and Tu, 1997; Whitehead et al, 2022).…”

Section: Resultsmentioning

confidence: 99%

“…In total, Drosophila is equipped with 12 flight steering muscles each of which likely contributes to a distinct function in flight control (Whitehead et al, 2022). The activation patterns of four of these muscles have been analyzed in response to optomotor stimulation during flight (first and second basalar muscles b1 and b2, as well as first pterale I muscle (i1) and the third pterale II muscle (iii1) (Heide and Götz, 1996; Dickinson and Tu, 1997; Whitehead et al, 2022). A schematic of these 4 direct flight muscles plus five adjacent ones that were analyzed in this study illustrates their spatial arrangement, shapes, and depicts which ones are innervated by steering MNs that express both aPKC (green) and FoxP (magenta), only one of both, or neither of them (grey; Fig.…”

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

“…Although the MN innervating the third basalar muscle, b2, also expresses aPKC along the axon, we did not detect aPKC signal in axon terminals or active zones, and it does not show FoxP label, thus ruling out a function of b2 in aPKC/FoxP mediated operant selflearning. In contrast to b1 and b3, b2 firing is not linked to the wingbeat cycle, but instead, it fires in bursts during turning maneuvers (Whitehead et al, 2022). Corroborating the conclusion that it is not involved in mediating operant self-learning, b2 is silent during straight flight, but it is likely involved in regulating body saccades (Heide, Götz, 1996) and Götz, 1996) and co-expresses aPKC and FoxP, whereas iii1 does reportedly (Heide and Götz, 1996) not participate in optomotor re- Plasticity in steering movements such as optomotor responses have been observed before, such as in classic "inversion goggles" experiments where the coupling between the fly's movements and the environment was reversed (Wolf and Heisenberg, 1986) or in a more recent experiment revealing adaptation processes (Mano et al, 2023).…”

Section: Motor Neurons Involved In Optomotor Responses Co-express Apk...mentioning

confidence: 91%

“…shown to be involved in generating optomotor responses (Heide and Götz, 1996;Whitehead et al, 2022), constitute a site of the plasticity mediating operant self-learning in Drosophila.…”

Section: Self-learning Breaks Optomotor Symmetrymentioning

confidence: 99%

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Wings of Change: aPKC/FoxP-dependent plasticity in steering motor neurons underlies operant selflearning inDrosophila

Ehweiner

Brembs

2022

Preprint

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Motor learning is not only a key invention of the many new animals evolving new body plans during the Cambrian, it is also central to human existence such as in learning to speak or walk, rehabilitation after injury, or sports. Evidence suggests that all forms of motor learning may share an evolutionary conserved molecular plasticity pathway. Here we present novel insights into the molecular processes underlying a kind of motor learning in the fruit fly Drosophila, operant self-learning. We have discovered that the Forkhead Box gene FoxP is not required in the fly brain for this type of learning. Instead, atypical protein kinase C (aPKC) appears to be a central component in a plasticity process that takes place in FoxP-expressing motor neurons in the ventral nerve cord. Using CRISPR/Cas9 to knock out canonical aPKC interaction partners bazooka and the kidney and brain gene (KIBRA) in adult animals, we found that aPKC likely acts via non-canonical pathways in this form of learning. We also found that 14 but not 7 days after CRISPR/Cas9-mediated knockout of FoxP in adult animals, learning is impaired, suggesting that adult FoxP expression is required for operant self-learning.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Motor Neurons Involved In Optomotor Responses Co-express Apk...mentioning

confidence: 91%

“…shown to be involved in generating optomotor responses (Heide and Götz, 1996;Whitehead et al, 2022), constitute a site of the plasticity mediating operant self-learning in Drosophila.…”

Section: Self-learning Breaks Optomotor Symmetrymentioning

confidence: 99%

See 3 more Smart Citations

Wings of Change: aPKC/FoxP-dependent plasticity in steering motor neurons underlies operant selflearning inDrosophila

Ehweiner

Brembs

2022

Preprint

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Synaptic architecture of leg and wing premotor control networks inDrosophila

Lesser

Azevedo

Phelps

et al. 2023

Preprint

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Animal movement is controlled by motor neurons (MNs), which project out of the central nervous system to activate muscles. Because individual muscles may be used in many different behaviors, MN activity must be flexibly coordinated by dedicated premotor circuitry, the organization of which remains largely unknown. Here, we use comprehensive reconstruction of neuron anatomy and synaptic connectivity from volumetric electron microscopy (i.e., connectomics) to analyze the wiring logic of motor circuits controlling theDrosophilaleg and wing. We find that both leg and wing premotor networks are organized into modules that link MNs innervating muscles with related functions. However, the connectivity patterns within leg and wing motor modules are distinct. Leg premotor neurons exhibit proportional gradients of synaptic input onto MNs within each module, revealing a novel circuit basis for hierarchical MN recruitment. In comparison, wing premotor neurons lack proportional synaptic connectivity, which may allow muscles to be recruited in different combinations or with different relative timing. By comparing the architecture of distinct limb motor control systems within the same animal, we identify common principles of premotor network organization and specializations that reflect the unique biomechanical constraints and evolutionary origins of leg and wing motor control.

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Flight power muscles have a coordinated, causal role in hawkmoth pitch turns

Wood,

Putney,

Sponberg

2023

Preprint

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Flying insects solve a daunting control problem of generating a patterned and precise motor program to stay airborne and generate agile maneuvers. In this motor program consisting of every action potential controlling wing musculature, each muscle encodes significant information about movement in precise spike timing down to the millisecond scale. While individual muscles share information about movement, we do not yet know if they have separable effects on an animal’s motion, or if muscles functionally interact such that the effects of any muscle’s timing depends heavily on the state of the entire musculature. To answer these questions, we performed spike-resolution electromyography and precise stimulation of individual spikes in the hawkmothManduca sextaduring tethered flapping. We specifically explored how the flight power muscles themselves may contribute to pitch control which is necessary to stabilize flight. Combining correlational study of visually-induced turns with causal manipulation of spike timing, we discovered likely coordination patterns for pitch turns, investigated if these correlational patterns can individually drive pitch control, and studied whether the precise spike timing of indirect power muscles can lead to pitch maneuvers. We observed significant timing change of the main downstroke muscles, the dorsolongitudinal muscles (DLMs), associated with whether a moth was pitching up or down. Causally inducing this timing change in the DLMs with electrical stimulation produced a consistent, mechanically relevant feature in pitch torque, establishing that indirect power muscles inManducahave a control role in pitch. Because changes were evoked in unconstrained flapping in only the DLMs, however, these pitch torque features left large unexplained variation. We find this unexplained variation indicates significant functional overlap in pitch control such that precise timing of one power muscle does not produce a precise turn, demonstrating the importance of coordination across the entire motor program for flight.Summary StatementWe investigate how individual muscles contribute to flight by manipulating muscle timing in behaving hawkmoths. We find precise timing of single muscles does not produce precise turns, highlighting the importance of coordination across the entire motor program.

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Neuromuscular embodiment of feedback control elements in Drosophila flight

Cited by 8 publications

References 71 publications

Wings of Change: aPKC/FoxP-dependent plasticity in steering motor neurons underlies operant selflearning inDrosophila

Wings of Change: aPKC/FoxP-dependent plasticity in steering motor neurons underlies operant selflearning inDrosophila

Synaptic architecture of leg and wing premotor control networks inDrosophila

Flight power muscles have a coordinated, causal role in hawkmoth pitch turns

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