Decoding the independent and synergistic roles of flight muscles for control of turning in the hawkmoth, Manduca sexta.
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1
University of Washington, Biology, United States
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2
Univeristy of Washington, Physiology and Biophysics, United States
To maneuver, organisms must not only acquire and process relevant sensory information, but transform that information into motor commands that alter movement dynamics. This motor decoding problem requires understanding how muscle forces and torques unfold continuously over time and against the background of ongoing body dynamics. Using insect flight as a model system we approach this decoding process by 1) identifying the task-relevant variation in forces and torques that arise from changing motor commands and 2) testing if these commands are distributed across multiple muscles in coordinated groups (e.g. synergies) for control. Many flying insects perform versatile turning maneuvers in a variety of ethological contexts, most notably for escape and to track and forage from wind-blown flowers while hovering. The traditional interpretation of flight control holds that insects like the hawkmoth, Manduca sexta, use large, dedicated power muscles activated with a single action potential during each wingstroke and maneuver using a suite of smaller steering muscles. We have recently shown that these large flight muscles have significant control authority via precise (sub-millisecond) modulation of the timing of these spikes. Yet what dynamics do these subtle changes in timing produce in order to create a net turn, and do the flight muscles have independent control during turning?
To address these questions, we recorded the patterns of muscle activations and torques during >3000 wingstrokes from six animals during left-right yawing responses to a moving visual stimulus. We first extracted the spike-triggered ensemble (STE) of torque waveforms for each wingstroke. Subsets of the STE for left- and right-most turns demonstrate that torque changes not only in its overall wingstroke-mean, but also in the shape of its within-stroke dynamics, particularly around ventral wingstroke reversal. To efficiently capture this change in shape and mean, we used a covariance analysis based on principle components (PCs) of the torque ensemble, but also applied a novel dimensionality reduction method based on projection onto latent structures (PLS or partial least squares). The PLS approach iteratively finds linear combinations (features) of the torque that maximally predict the timing changes in muscle activation, thereby ignoring variation in torque that is unrelated to the changing motor commands. We found that yaw turning is well described with only two underlying PLS torque features. We used this task-relevant description of variation to more rigorously test the independent role of each of the flight downstroke muscles. An earlier analysis using typical summary statistics of torque (e.g. the wingstroke mean) supported the synergistic role of these muscles and failed to predict the within-stroke torque dynamics. The PLS feature analysis rejects these conclusions, more accurately predicting the continuous torque dynamics and showing that the two muscles have significant independent contributions to control. Insect flight control, with its analytically tractable motor activations and accessible dynamics, is advantageous for tackling questions of how motor control is distributed, coordinated and decoded in intact, locomoting animals. Applying computational approaches, such as PLS feature analysis, in this context reveals the control authority of multiple muscles.
Keywords:
dimensionality reduction,
flight,
insect,
Manduca,
motor control,
Muscle,
optomotor,
Synergy
Conference:
Tenth International Congress of Neuroethology, College Park. Maryland USA, United States, 5 Aug - 10 Aug, 2012.
Presentation Type:
Poster (but consider for participant symposium and student poster award)
Topic:
Motor Systems
Citation:
Sponberg
S,
Fairhall
AL and
Daniel
TL
(2012). Decoding the independent and synergistic roles of flight muscles for control of turning in the hawkmoth, Manduca sexta..
Conference Abstract:
Tenth International Congress of Neuroethology.
doi: 10.3389/conf.fnbeh.2012.27.00350
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Received:
30 Apr 2012;
Published Online:
07 Jul 2012.
*
Correspondence:
Dr. Simon Sponberg, University of Washington, Biology, Seattle, WA, 98195-1800, United States, bergs@u.washington.edu