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

authors: Theodore Lindsay, Anne Sustar, Michael Dickinson
doi: 10.1016/j.cub.2016.12.018

CITATION

Lindsay, T., Sustar, A., & Dickinson, M. (2017). The Function and Organization of the Motor System Controlling Flight Maneuvers in Flies. Current Biology, 27(3), 345–358. https://doi.org/10.1016/j.cub.2016.12.018

ABSTRACT

fleeting notes


how do sparse motor systems produce fast maneuvers and fine scaled adjustments

direct muscles connect to sclerites - tiny hardened cuticle which acts like skeletal elements
wing hinge is very complicated

steering muscles segregate into 4 major groups based on the sclerites that they insert into

  1. basalars - (b1, b2, b3)
  2. first axillaries - (i1, i2)
  3. third axillaries - (iii1, iii3, iii4) - iii2 is missing in drosophila
  4. fourth axillaries - (hg1, hg2, hg3, hg4)

imaged calcium activity of the muscles during different visual stimuli

each anatomical group of steering muscles contains 2 functionally distinct activity profiles
each anatomical group of steering muscles contains 2 functional classes

  1. phasic muscles that generate large transient changes
  2. tonic muscles that regulate continuously

focused on a sagittal plane under surface of cuticle to capture many steering muscles at once

  • the muscles overlap so could not define ROIs for every muscle
  • used a manually segmented anatomical model to extract ROIs
  • muscles that clustered together and had overlap were part of the same anatomical class

at flight initiation and cessation all steering muscles increase activity

some muscles decayed to zero at steady state flight

ispilateral saccades - increase in b3, i1, hg1 and hg4 and decrease of iii3
contralateral saccades - b2, iii1 increase and b3 decreases

most of the phasic muscles are the largest of their anatomical group
phasic muscles are inactive most of the time

during saccades the tonic muscles are recruited linearly, phasic muscles are recruited non linearly
3 categories of muscles during saccades:

  • linear activity with saccade amplitude - suggesting fine tuning magnitude of each turn
    • b1, b3, iii3, hg4
  • strong rectification of muscles - recruited only during largest saccades in one direction
    • b2, i1, iii1, hg1
  • the last group is mostly flat but have some trends similar to rest of anatomical group
    • i2, iii4, hg2, hg3

each anatomical group has one muscle that is active during largest saccade and at least one muscle that had graded control over wing motion (phasic and tonic)

regressed each muscle signal against stroke amplitude for every flight trial

  • essentially a linear model for muscle activity and stroke amplitude
  • the more muscles they include in the model, the more variance explained

muscle best fit = iii3 which is a tonic muscle and follows the slow modulations of stroke amplitude but does not capture fast saccades

  • all muscles contribute to stroke amplitude but some only are used during saccades so

visual motion drives 2 independent processes

  • one carries motor commands for slow responses (tonic muscles)

  • one has stochastic commands for random turns (phasic muscles)

  • tonic muscles would be sensitive to small inputs from integrator pathway and large inputs from saccade pathway

  • phasic muscles are typically hyperpolarized below threshold and only respond to large transient signals like saccades or large optomotor responses

b1 and b2 = extend the ventral extreme of the wing stroek amplitude
b3 = extend the dorsal extreme

  • these change the pitch axis of the fly (nose up or down)
    i1 and ii2 = depress stroke plane ventrally
    iii1, iii3 and iii4 = antagonists to i1 and i2, elevate stroke plane and incerase stroke amplitude
    hg muscles regulate angle of attack for production of yaw torque

there is a mechanical clutch that engages and disengages the wing

  • iii1 has largest activation at cessation of flight when animal folds its wings

highlights


To identify strategies by which animals execute precise actions using sparse motor networks, we imaged the activity of a complete ensemble of wing control muscles in intact, flying flies.Page 2

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