Neural Coding of Leg Proprioception in Drosophila

authors: Akira Mamiya, Pralaksha Gurung, John C. Tuthill
doi: 10.1016/j.neuron.2018.09.009

CITATION

Mamiya, A., Gurung, P., & Tuthill, J. C. (2018). Neural Coding of Leg Proprioception in Drosophila. Neuron, 100(3), 636-650.e6. https://doi.org/10.1016/j.neuron.2018.09.009

ABSTRACT

fleeting notes


  • 2p calcium imaging of proprioceptive sensory neurons during controlled movements of the fly tibia

  • axons are organized into distinct functional projections containing topographic representations of kinematic features — does this just mean movement?

  • one group = tibia position (flexion and extension)

  • one group = tibia movement direction

  • one group = tibia bidirectional movement and vibration frequency

  • “proprioceptive stimuli from single leg joint are encoded by diverse population of sensory neurons and how proprioceptive feedback signals are used by motor circuits to coordinate body”

  • proprioception

  • Femoral chordotonal organ - FeCO

  • population imaging from proprioceptive neurons labeled by iav-gal4

  • chose to control leg kinematics with a magnetic bar that moved the joint angle

  • calculated pairwise correlations between calcium signal in each pixel in order to cluster activity then performed kmeans clustering on the correlation matrix

    • this revealed spatially separated groups of axons that encode distinct proprioceptive stim features
  • to find the functional organization of FeCO axons

    • first clustered trial to trial from four regions of interest
    • combined responses from same region in different flies
    • then grouped again using kmeans clustering
  • 5 basic subclasses of responses in FeCO axons

    • two tonic non adapting
    • 3 phasic adapting
  • tonic response - increase activity when tibia extends or flexes

  • phasic response - transient increase during movement phase of swing

    • one responded to either direction
    • 2 responded only to one direction
  • different projections of proprioceptive axons have different tuning and are organized similarly across flies

  • club - labels axons that run laterally through center of leg (R64C04-Gal4)

    • terminate near midline. some toward brain or other segments
  • claw - shaped like a claw. projections split into 3 smaller branches. X,Y,Z branches. (R73D10-Gal4)

  • hook - projections run along Z branch of the claw and extend a longer arborization toward midline (R21D21-Gal4)

  • proprioceptor driver lines

  • claw neurons tonically increase activity in response to flexion or extension of tibia

  • club neurons phasically increase activity in response to flexion or extension

  • hook neurons active more during flexion

  • ramp and hold stimulus to explore position dependent tuning of proprioceptor subclasses

    • claw neurons responded with tonic increases during flexion or extension
      • activity of extension tuned pixels increased when tibia was between 90 and 180 degrees
      • flexion tuned pixels increased when tibia was less than 90 degrees
      • none active during middle of range
      • linear tuning of femur tibia joint angle
    • club neurons respond phasically to each tibia movement regardless of direction across all joint angles
    • hook neurons phasically increase activity during flexion not extension. slightly weaker when fully extended
  • used a piezoelectric chip to vibrate magnet attached to leg at different frequencies (100-2000 hz)

  • club neurons have large response to tibia vibration

  • claw and hook do not respond to vibration

  • spatial organization of responses in club neurons in response to frequency range

    • a frequency map
  • single club neurons are tuned to different frequencies

  • single claw neurons are tuned to have peak responses at different femur tibia angles

claw neurons encode the position of the tibia

highlights


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