Skip to main content
Advertisement

Main menu

  • Home
  • Articles
    • Accepted manuscripts
    • Issue in progress
    • Latest complete issue
    • Issue archive
    • Archive by article type
    • Special issues
    • Subject collections
    • Interviews
    • Sign up for alerts
  • About us
    • About JEB
    • Editors and Board
    • Editor biographies
    • Travelling Fellowships
    • Grants and funding
    • Journal Meetings
    • Workshops
    • The Company of Biologists
    • Journal news
  • For authors
    • Submit a manuscript
    • Aims and scope
    • Presubmission enquiries
    • Article types
    • Manuscript preparation
    • Cover suggestions
    • Editorial process
    • Promoting your paper
    • Open Access
    • Outstanding paper prize
    • Biology Open transfer
  • Journal info
    • Journal policies
    • Rights and permissions
    • Media policies
    • Reviewer guide
    • Sign up for alerts
  • Contacts
    • Contact JEB
    • Subscriptions
    • Advertising
    • Feedback
  • COB
    • About The Company of Biologists
    • Development
    • Journal of Cell Science
    • Journal of Experimental Biology
    • Disease Models & Mechanisms
    • Biology Open

User menu

  • Log in

Search

  • Advanced search
Journal of Experimental Biology
  • COB
    • About The Company of Biologists
    • Development
    • Journal of Cell Science
    • Journal of Experimental Biology
    • Disease Models & Mechanisms
    • Biology Open

supporting biologistsinspiring biology

Journal of Experimental Biology

  • Log in
Advanced search

RSS  Twitter  Facebook  YouTube  

  • Home
  • Articles
    • Accepted manuscripts
    • Issue in progress
    • Latest complete issue
    • Issue archive
    • Archive by article type
    • Special issues
    • Subject collections
    • Interviews
    • Sign up for alerts
  • About us
    • About JEB
    • Editors and Board
    • Editor biographies
    • Travelling Fellowships
    • Grants and funding
    • Journal Meetings
    • Workshops
    • The Company of Biologists
    • Journal news
  • For authors
    • Submit a manuscript
    • Aims and scope
    • Presubmission enquiries
    • Article types
    • Manuscript preparation
    • Cover suggestions
    • Editorial process
    • Promoting your paper
    • Open Access
    • Outstanding paper prize
    • Biology Open transfer
  • Journal info
    • Journal policies
    • Rights and permissions
    • Media policies
    • Reviewer guide
    • Sign up for alerts
  • Contacts
    • Contact JEB
    • Subscriptions
    • Advertising
    • Feedback
Research Article
The free-flight response of Drosophila to motion of the visual environment
Markus Mronz, Fritz-Olaf Lehmann
Journal of Experimental Biology 2008 211: 2026-2045; doi: 10.1242/jeb.008268
Markus Mronz
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Fritz-Olaf Lehmann
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • Article
  • Figures & tables
  • Supp info
  • Info & metrics
  • PDF
Loading

Article Figures & Tables

Figures

  • Fig. 1.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Fig. 1.

    Experimental apparatus and flight path analysis. (A) Flight arena for measuring free-flight performance in Drosophila under optomotor stimulus conditions. A gear motor rotates the visual environment at distinct angular velocities, and three circular fluorescent light tubes (FLT) illuminate the visual pattern from behind. The flies are automatically released into the arena bottom (outlet) via a microprocessor-controlled gate. A high-speed video camera is triggered when the animal takes off, and cardboard shields the experimental setup from ambient light. (B) Estimation of flight altitude. Pictograms show typical video images of unrestrained animals flying at various altitudes. The red borderline outlines the fly body (oval blob), the inner dot indicates the centre of mass, and the line shows body orientation. Plotted data are derived from a tethered fly that is vertically moved by hand inside the middle of the arena. Red line shows linear regression fit. Means ± s.d.; N=10 flies. (C) Random dot pattern used in the experiments. (D) The fly's gaze (β) is defined as the angle between 0° direction and a line running through the arena centre and the point of path convergence projected on the outer pattern cylinder. (E) Angular velocity of the animal is calculated from the temporal change in angular orientation (dα/dt) given by three successive data points within the x/y coordinate system. r, path radius; t, time.

  • Fig. 2.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Fig. 2.

    Side-slip manoeuvre of Drosophila and body orientation. (A) Sequence of video images showing a side-slip manoeuvre of a flying fruit fly in front of the rotating pattern. The red arrow indicates body orientation that is derived from the length and width ratio of the fly's image (grey blob). The small red dot indicates the position of the fly's head. Sampling rate, 62.5 Hz; rotational speed of environment, 180° s–1. (B) Data of a single fly showing the relationship between body orientation derived from blob analysis (x-scale, orientation I, b/a ratio <0.8, where b is the lateral and a the longitudinal extension of the blob ellipsis, inset) and body orientation reconstructed from the position of the fly on two successive video frames (y-scale, orientation II). In the experiment, the fly responded to an optomotor pattern rotating at 500° s–1. Flight time was 7.54 s. Linear regression fit (reduced major axis, model II regression, y=0.995x–2.12, R2=0.94, N=775 sample points, P<0.001, red) shows a high degree of conformance between the two methods, suggesting that side-slip manoeuvres are rare in freely flying Drosophila. See text for details.

  • Fig. 3.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Fig. 3.

    Mean position probability of freely flying fruit flies at various rotational velocities of the flight arena (bin width, 4 mm×4 mm). (A) Stationary pattern. (B) 100, (C) 300, (D) 500, (E) 700 and (F) 900° s–1 arena velocity. The outer rings represent the random-square pattern while the white line marks the position of the immovable translucent inner cylinder. All position histograms are normalized to the same data sum and position probability is plotted in pseudo-colour.

  • Fig. 4.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Fig. 4.

    Distance between the animal and the arena centre, and turning angles at various experimental conditions. (A) Probability histograms and medians (dotted white lines) of the distributions obtained for flies responding to six different arena velocities. Means ± s.e.m. (B) Mean distance of the flying animal from the arena centre plotted against the fly's horizontal (forward) velocity (bin width, 0.1 m s–1). Linear regression fit is plotted in red (y=0.016x+35.8, R2=0.88, N=13 horizontal velocity bins, P<0.001). (C) Total turning angle within a flight saccade (grey) and between two saccades (open) shown as a function of arena velocity. (D) Ratio of total turning angle during saccadic flight style and smooth turning between two subsequent saccades. Data show a minimum contribution of saccades to turning angle at 500° s–1 arena velocity. SMT, time between two flight saccades; SAT, duration of a saccade. Means ± s.d., N=131 flies.

  • Fig. 5.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Fig. 5.

    Mean flight velocities at various rotational velocities of the flight arena. Mean horizontal (black, left scale), turning (blue, right scale) and vertical (red, left scale) velocity of the animals in response to the changes in stimulus conditions. The fly may fully achieve retinal slip compensation (grey area) when angular velocity, which is the rate of change in gaze, is equal to the angular speed of the rotating environment at a given horizontal velocity (slope=1, dotted blue). Positive turning and vertical values mean counter-clockwise turns and climbing flight, respectively; N=22 (0° s–1), 23 (100° s–1), 20 (300° s–1), 20 (500° s–1), 21 (700° s–1) and 26 flies (900° s–1). Means ± s.e.m.

  • Fig. 6.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Fig. 6.

    Saccadic flight style of Drosophila flying freely in a non-rotating random-dot arena. (A–C) Three flight paths of single fruit flies voluntarily starting from rest (top view). Flight is characterized by sequences of straight flight interspaced by 130 ms short, approximately 90–180° saccadic turns. Horizontal forward velocity is plotted in pseudo-colour. Red cross, arena centre. (D) Angular velocity during flight saccades elicited at various forward velocities in response to optomotor stimulation. Each data point of a curve represents the averaged value derived from the mean saccadic velocity of each of the 131 tested fruit flies. The mean standard deviations over all data points of each curve amount to 546 (black), 425 (red), 347 (green), 263 (blue), 287 (cyan) and 513° s–1 (purple). (E) Modulation in horizontal velocity during flight saccades. The standard deviations averaged over all data points of a curve amount to 0.12 (black), 0.12 (red), 0.15 (green), 0.10 (blue), 0.13 (cyan) and 0.17 m s–1 (purple). (F) Frequency of saccades slightly increases with increasing horizontal velocity estimated from flight sequences between saccades (intersaccade velocity). The black line represents the linear regression fit on the data set (y=1.31x+2.55, R2=0.04, N=131 saccades, P=0.024). Colour coding in D–F: 0° s–1, 0.26±0.08 m s–1, 22 (black); 100° s–1, 0.27±0.08 m s–1, 23 (red); 300° s–1, 0.33±0.07 m s–1, 20 (green); 500° s–1, 0.45±0.06 m s–1, 20 (blue); 700° s–1, 0.49±0.09 m s–1, 21 (cyan); and 900° s–1, 0.45±0.09 m s–1, 26 (purple); for arena velocity, mean forward flight velocity and number of flies, respectively.

  • Fig. 7.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Fig. 7.

    Gaze and response of a rotation-sensitive elementary motion detector (EMD) system for two single flies flying in a stationary random-dot environment (A–E) and under optomotor stimulation due to the rotating arena (500° s–1 counter-clockwise rotation, F–J). The time traces in B–E and G–J are subsets of the flight sequences in A and F. (A,F) Flight path and EMD response (left-minus-right eye) plotted in pseudo-colour for both stimulus conditions. Red cross, arena centre. (B,G) The fly's gaze was derived according to the procedure shown in Fig. 1D. The movement of the cylinder panorama (infrared light marker) is shown in red (right scale). (C,H) EMD response of left (blue) and right (red) eye derived according to the position and speed of the fly inside the arena and the visual panorama. (D,I) Left-minus-right eye EMD response (black) and turning velocity (red), and (E,J) left-plus-right eye EMD response (black) and horizontal velocity (red) are plotted for both stimulus conditions. Upper dotted line in D and I indicates the threshold used to identify flight saccades (>1000° s–1). Grey dots indicate times at which flight saccades occur. Black, left scale; red, right scale.

  • Fig. 8.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Fig. 8.

    Close-up of the flight sequence in a stationary arena cylinder (left turn). (A) The fly's gaze calculated from body orientation. (B) Inverse relationship between horizontal (blue, right scale) and turning (red, right scale) velocity, and output of a rotation-sensitive EMD system (left-minus-right eye, black, left scale).The sum of EMD responses of the two eyes is plotted in grey (left scale). Light grey area indicates times at which the fly exhibits approximately constant gaze in A and saccades in B.

  • Fig. 9.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Fig. 9.

    Histograms of responses of a rotation-sensitive EMD system for flight sequences produced by flies flying in a stationary environment and during optomotor stimulation. (A) Distribution of the mean value bins (grey) and standard errors of left-minus-right eye EMD output of flies responding to various arena velocities. (B) Histograms show the sum of EMD output (left-plus-right eye) derived from the same flight data as shown in A. Gaussian fits to each histogram are shown as solid red lines. All histograms are normalized to the same area under the curve.

  • Fig. 10.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Fig. 10.

    Outputs of two EMD system types in freely flying fruit flies. (A) According to previous findings on yaw torque production in tethered flies, we simulated a rotation-sensitive EMD system (upper pictogram) and an expansion-sensitive system with a lateral focus of expansion (lower pictogram). (B,C) Relative mean EMD output of the rotation system estimated from the Gaussian fit to the histograms shown in Fig. 9A and B, respectively. Errors represent the standard deviation of the fit, which is 0.5 the width of the Gaussian curve at half-peak height. Data in B and C show the mean difference (left-minus-right eye) and sum (left-plus-right eye) of the EMD response between the two eyes, respectively. (D) Relative mean EMD output (left-minus-right eye) of an expansion-sensitive system estimated from Gaussian fits similar to those shown in Fig. 9A,B. (E,F) EMD response of the rotation (black)- and expansion (red)-sensitive EMD system in flight sequences derived from two flies flying in a stationary environment in E and during 300° s–1 arena velocity in F. See text for details. cw, clockwise turning (grey area); cww, counter clockwise turning.

  • Table 1.

    Linear regression fit statistics between the fly's turning velocity and the left-minus-right eye output of the rotation- and expansion-sensitive elementary motion detector system, respectively

    Arena velocity (° s–1)EMD systemSlope × 10–3y-interceptR2PN
    0Rotation–2.51±2.710.02±1.020.12±0.120.13±0.23 (NS)22
    100Rotation–4.00±0.420.77±0.190.23±0.090.003±0.009**23
    300Rotation–4.63±1.161.50±0.430.36±0.110.004±0.01**20
    500Rotation–5.40±1.022.57±0.440.47±0.11<0.0001***20
    700Rotation–4.38±0.722.68±0.450.34±0.120.03±0.14*21
    900Rotation–1.76±2.261.60±1.060.06±0.050.22±0.23 (NS)26
    0Expansion–0.21±1.080.10±0.330.07±0.100.34±0.29 (NS)22
    100Expansion–0.50±1.100.20±0.370.04±0.040.26±0.32 (NS)23
    300Expansion0.64±1.42–0.25±0.580.10±0.120.15±0.23 (NS)20
    500Expansion1.05±1.85–0.51±0.940.06±0.070.18±0.29 (NS)20
    700Expansion0.60±1.90–0.33±0.990.03±0.040.29±0.34 (NS)21
    900Expansion–0.33±1.590.18±0.700.04±0.040.35±0.32 (NS)26
    • We performed model I regression fit on a data subset ranging from 0 to 900° s–1 turning velocity. *0.05, **0.01 and ***0.001 significance level of slope. NS, not significant. N, number of flies. Data are means ± s.d.

  • Fig. 11.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Fig. 11.

    Relationships between flight path curvature, horizontal and turning velocity in freely flying fruit flies. (A) The variance in flight path curvature decreases with increasing horizontal velocity. At maximum forward velocity of approximately 1.0 m s–1, flight path curvature is apparently constrained to a unique value of approximately 0.016 mm–1. (B) Relationship between flight path curvature and turning velocity. (C) Data distribution between horizontal and angular velocity. Each data point represents an 8 ms position measurement of each of the tested flies. The vertical line in C indicates maximum horizontal velocity of 0.49 m s–1 averaged over all flies. Normalized relative frequencies are plotted in pseudo-colour.

  • Fig. 12.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Fig. 12.

    Numerical model for force balance in freely flying fruit flies. (A) Forces produced by the flying insect and forces acting on the fly body during flight on a curved path. Total flight force Ft is equal to the vector sum of horizontal (Fh), vertical (Fv) and lateral forces (Fl). (B) Total force of each fly and the corresponding force components within the flight recordings that fell within the top 10% maximum of total force. Data are sorted after Ft for all 131 tested animals. (C) Minimum flight path radius at a given forward velocity and level flight, shown for four estimates of total flight force. (D) Alterations in vertical climbing velocity when horizontal flight velocity is kept constant at 0.6 m s–1. Grey indicates path radii at which the fly loses flight altitude while turning. The numerical model predicts that at 0.6 m s–1 forward speed fruit flies may only support their body weight when the flight path radius exceeds 50 mm (dotted line). Fg, gravitational force (body weight); CoR, centre of radius of a flight turn; r, radius of the flight path; ul, lateral (side-slip) velocity; uh, horizontal velocity; uv,max, maximum vertical velocity.

  • Fig. 13.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Fig. 13.

    Force components and body velocities of single flies flying freely in a stationary (left) and rotating (500° s–1, right) random-dot flight arena. (A,F) Flight paths of the two animals lasting 2.4 s each. Horizontal (B,G), vertical (C,H), centripetal (D,I) and total (E,J) forces (black, left scale) and velocities (red, right scale), measured from the fly's body motion inside the arena and calculated from the equations given in the text, respectively. Total velocity is the vector sum of horizontal, vertical and turning velocity. Grey dots indicate saccades in which turning velocity exceeds 1000° s–1 angular speed. Red cross, centre of flight arena.

  • Fig. 14.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Fig. 14.

    Relationship between horizontal velocity and lateral force during turning in freely manoeuvring Drosophila. Data points for horizontal velocity (A) and lateral force (B) are plotted against flight path radius, whereas relative frequency is shown in pseudo-colour. Graphs show superimposed data derived from all tested flies. (C) Binned means for horizontal velocity (black, left scale) and lateral (centripetal) force (blue, right scale) derived from the data shown in A and B. N=131 flies. Means ± s.d. Radius of the inner cylinder of the arena was 70 mm.

  • Fig. 15.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Fig. 15.

    Behavioural data and maximum velocity estimates for flight derived from high-speed video analysis and a numerical model on force balance in flying fruit flies, respectively. Distributions of horizontal (A) and turning (B) velocities were derived in a stationary environment and during optomotor stimulation (N=131 flies). The means and 95% quantiles of 20 data bins (bin width, 10 mm path radius) are plotted in red and blue, respectively. The 95% quantile fairly describes the upper border of the data distribution. The black lines in C and D represent the model estimates based on the four maximum total flight force values mentioned in the Results. The model values were calculated assuming no change in the fly's vertical position. Red and blue in C and D are re-plotted from A and B, respectively. Dotted lines indicate the diameter of the inner cylinder (70 mm).

Previous ArticleNext Article
Back to top
Previous ArticleNext Article

This Issue

 Download PDF

Email

Thank you for your interest in spreading the word on Journal of Experimental Biology.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
The free-flight response of Drosophila to motion of the visual environment
(Your Name) has sent you a message from Journal of Experimental Biology
(Your Name) thought you would like to see the Journal of Experimental Biology web site.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Share
Research Article
The free-flight response of Drosophila to motion of the visual environment
Markus Mronz, Fritz-Olaf Lehmann
Journal of Experimental Biology 2008 211: 2026-2045; doi: 10.1242/jeb.008268
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Research Article
The free-flight response of Drosophila to motion of the visual environment
Markus Mronz, Fritz-Olaf Lehmann
Journal of Experimental Biology 2008 211: 2026-2045; doi: 10.1242/jeb.008268

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Alerts

Please log in to add an alert for this article.

Sign in to email alerts with your email address

Article navigation

  • Top
  • Article
    • SUMMARY
    • INTRODUCTION
    • MATERIALS AND METHODS
    • RESULTS
    • DISCUSSION
    • CONCLUSIONS
    • APPENDIX
    • ACKNOWLEDGEMENTS
    • FOOTNOTES
    • References
  • Figures & tables
  • Supp info
  • Info & metrics
  • PDF

Related articles

Cited by...

More in this TOC section

  • Departures from isotropy: the kinematics of a larval snail in response to food
  • Trunk and leg kinematics of grounded and aerial running in bipedal macaques
  • The visual ecology of Holocentridae, a nocturnal coral reef fish family with a deep-sea-like multibank retina
Show more RESEARCH ARTICLE

Similar articles

Other journals from The Company of Biologists

Development

Journal of Cell Science

Disease Models & Mechanisms

Biology Open

Advertisement

Meet the Editors at SICB Virtual 2021

Reserve your place to join some of the journal editors, including Editor-in-Chief Craig Franklin, at our Meet the Editor session on 17 February at 2pm (EST). Don’t forget to view our SICB Subject Collection, featuring relevant JEB papers relating to some of the symposia sessions.


2020 at The Company of Biologists

Despite 2020's challenges, we were able to bring a number of long-term projects and new ventures to fruition. As we enter a new year, join us as we reflect on the triumphs of the last 12 months.


Critical temperature window sends migratory black-headed buntings on their travels

The spring rise in temperature at black-headed bunting overwintering sites is essential for triggering the physical changes that they undergo before embarking on their spring migration – read more.


Developmental and reproductive physiology of small mammals at high altitude

Cayleih Robertson and Kathryn Wilsterman focus on high-altitude populations of the North American deer mouse in their review of the challenges and evolutionary innovations of pregnant and nursing small mammals at high altitude.


Read & Publish participation extends worldwide

“Being able to publish Open Access articles free of charge means that my article gets maximum exposure and has maximum impact, and that all my peers can read it regardless of the agreements that their universities have with publishers.”

Professor Roi Holzman (Tel Aviv University) shares his experience of publishing Open Access as part of our growing Read & Publish initiative. We now have over 60 institutions in 12 countries taking part – find out more and view our full list of participating institutions.

Articles

  • Accepted manuscripts
  • Issue in progress
  • Latest complete issue
  • Issue archive
  • Archive by article type
  • Special issues
  • Subject collections
  • Interviews
  • Sign up for alerts

About us

  • About JEB
  • Editors and Board
  • Editor biographies
  • Travelling Fellowships
  • Grants and funding
  • Journal Meetings
  • Workshops
  • The Company of Biologists
  • Journal news

For Authors

  • Submit a manuscript
  • Aims and scope
  • Presubmission enquiries
  • Article types
  • Manuscript preparation
  • Cover suggestions
  • Editorial process
  • Promoting your paper
  • Open Access
  • Outstanding paper prize
  • Biology Open transfer

Journal Info

  • Journal policies
  • Rights and permissions
  • Media policies
  • Reviewer guide
  • Sign up for alerts

Contact

  • Contact JEB
  • Subscriptions
  • Advertising
  • Feedback

 Twitter   YouTube   LinkedIn

© 2021   The Company of Biologists Ltd   Registered Charity 277992