title: Frequency response of lift control in Drosophila.
abstract: The flight control responses of the fruitfly represent a powerful model system to explore neuromotor control mechanisms, whose system level control properties can be suitably characterized with a frequency response analysis. We characterized the lift response dynamics of tethered flying Drosophila in presence of vertically oscillating visual patterns, whose oscillation frequency we varied between 0.1 and 13 Hz. We justified these measurements by showing that the amplitude gain and phase response is invariant to the pattern oscillation amplitude and spatial frequency within a broad dynamic range. We also showed that lift responses are largely linear and time invariant (LTI), a necessary condition for a meaningful analysis of frequency responses and a remarkable characteristic given its nonlinear constituents. The flies responded to increasing oscillation frequencies with a roughly linear decrease in response gain, which dropped to background noise levels at about 6 Hz. The phase lag decreased linearly, consistent with a constant reaction delay of 75 ms. Next, we estimated the free-flight response of the fly to generate a Bode diagram of the lift response. The limitation of lift control to frequencies below 6 Hz is explained with inertial body damping, which becomes dominant at higher frequencies. Our work provides the detailed background and techniques that allow optomotor lift responses of Drosophila to be measured with comparatively simple, affordable and commercially available techniques. The identification of an LTI, pattern velocity dependent, lift control strategy is relevant to the underlying motion computation mechanisms and serves a broader understanding of insects' flight control strategies. The relevance and potential pitfalls of applying system identification techniques in tethered preparations is discussed.
authors.affiliation: Institute of Robotics and Intelligent Systems, ETH Zurich, Zurich, Switzerland.
authors.forename: Chauncey F
authors.initials: CF
authors.lastname: Graetzel
authors.forename: Bradley J
authors.initials: BJ
authors.lastname: Nelson
authors.forename: Steven N
authors.initials: SN
authors.lastname: Fry
mesh_terms: D000818:Animals; D001696:Biomechanical Phenomena; D004331:Drosophila melanogaster / Q000502:physiology*; D056228:Feedback, Sensory; D005260:Female; D005426:Flight, Animal / Q000502:physiology*; D016014:Linear Models; D008297:Male; D010775:Photic Stimulation
references.citation: Trends Neurosci. 1989 Aug;12(8):297-306
references.pmid: 2475948
references.citation: Curr Biol. 2009 Jan 13;19(1):R36-47
references.pmid: 19138592
references.citation: J Exp Biol. 2002 Apr;205(Pt 8):1087-96
references.pmid: 11919268
references.citation: Kybernetik. 1968 Jun;4(6):199-208
references.pmid: 5731498
references.citation: J R Soc Interface. 2011 Feb 6;8(55):171-85
references.pmid: 20525744
references.citation: Science. 2003 Apr 18;300(5618):495-8
references.pmid: 12702878
references.citation: Curr Biol. 2007 Feb 20;17(4):329-35
references.pmid: 17291757
references.citation: J Neurosci Methods. 2008 Jan 30;167(2):127-39
references.pmid: 17854905
references.citation: J Exp Biol. 1997 Apr;200(Pt 7):1133-43
references.pmid: 9131808
references.citation: J Exp Biol. 1996;199(Pt 1):237-44
references.pmid: 9317712
references.citation: Biol Cybern. 1999 Feb;80(2):109-16
references.pmid: 12440388
references.citation: Curr Opin Neurobiol. 2004 Dec;14(6):729-36
references.pmid: 15582376
references.citation: J Exp Biol. 2008 Jul;211(Pt 13):2026-45
references.pmid: 18552291
references.citation: J Exp Biol. 2007 Dec;210(Pt 24):4319-34
references.pmid: 18055621
references.citation: J Exp Biol. 2005 Jun;208(Pt 12):2303-18
references.pmid: 15939772
references.citation: Curr Biol. 2008 Mar 11;18(5):368-74
references.pmid: 18328703
references.citation: J Exp Biol. 2002 Sep;205(Pt 18):2785-98
references.pmid: 12177144
references.citation: J Exp Biol. 1999 Jun;202 (Pt 11):1481-90
references.pmid: 10229694
references.citation: J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2002 Jul;188(6):419-37
references.pmid: 12122462
references.citation: J Neurosci Methods. 2008 Jun 15;171(1):110-7
references.pmid: 18405978
references.citation: J Exp Biol. 2003 Jan;206(Pt 2):295-302
references.pmid: 12477899
references.citation: Br J Psychol. 1958 Aug;49(3):182-94
references.pmid: 13572790
references.citation: Curr Biol. 2008 Apr 22;18(8):R339-41
references.pmid: 18430633
references.citation: J Exp Biol. 2008 Feb;211(Pt 3):341-53
references.pmid: 18203989
references.citation: J Exp Biol. 2010 Apr;213(Pt 8):1366-75
references.pmid: 20348349
references.citation: Int Rev Neurobiol. 2000;44:93-120
references.pmid: 10605643
references.citation: J Exp Biol. 2006 Nov;209(Pt 22):4533-45
references.pmid: 17079723
references.citation: J Exp Biol. 2010 Feb 15;213(4):602-12
references.pmid: 20118311
references.citation: Trends Neurosci. 2002 Feb;25(2):96-102
references.pmid: 11814562
references.citation: Rev Oculomot Res. 1993;5:239-63
references.pmid: 8420551
references.citation: J Neurophysiol. 2006 Sep;96(3):1602-14
references.pmid: 16687623
references.citation: Curr Opin Neurobiol. 2002 Dec;12(6):699-706
references.pmid: 12490262
references.citation: J Exp Biol. 2009 Apr;212(Pt 8):1120-30
references.pmid: 19329746
references.citation: Nature. 1998 Oct 15;395(6703):654
references.pmid: 9790186
references.citation: Neuron. 2008 Jul 31;59(2):322-35
references.pmid: 18667159
references.citation: J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2007 Jul;193(7):787-99
references.pmid: 17551735
references.citation: Science. 2009 Apr 10;324(5924):252-5
references.pmid: 19359586
references.citation: Curr Biol. 2006 May 9;16(9):R309-14
references.pmid: 16682333
references.citation: Vision Res. 1999 Aug;39(16):2749-66
references.pmid: 10492835
references.citation: Kybernetik. 1973 May;12(4):185-203
references.pmid: 4718020