SummaryA recent study sheds new light on the visual cues used by Drosophila to regulate flight altitude. The striking similarity with previously identified steering mechanisms provides a coherent basis for novel models of vision-based flight control in insects and robots

Floreano, Dario

Zufferey, Jean-Christophe

A recent study sheds new light on the visual cues used by Drosophila to regulate flight altitude. The striking similarity with previously identified steering mechanisms provides a coherent basis for novel models of vision-based flight control in insects and robots

Infoscience - École polytechnique fédérale de Lausanne

DispatchR847binding. Furthermore, as acetylationoccurs only after microtubulepolymerization, the enzymeresponsible for this modificationshould probably localize to themicrotubule lumen.The preference of ER sliding foracetylated microtubules may indicatea functional difference between thistype of ER motility and that mediatedby the tip attachment complex.Intermembrane contacts are importantfor many functions of the ER andother membranous compartments [9].The authors’ results led them tohypothesize that the slidingmechanism may be used as a wayfor ER tubules to find and contact otherorganelles along a subpopulationof microtubules.To explore this possibility, Friedmanet al. [8] tracked the movements of twoother organelles, mitochondria andendosomes, with respect to both ERand acetylated microtubules. Amajority of both organelles remainedin persistent contact with the ER.However, only mitochondria appearedto also localize preferentially toacetylated microtubules, suggestingthat ER contacts with mitochondria,but not endosomes, are enriched alongacetylated microtubules. Consistentwith this finding is the fact that both ERand mitochondria are cargoes ofkinesin-1, while endosomes are movedby KIF16B, a member of the kinesin-3family [15]. Further, work byCai et al. [6]showed that another kinesin-3 familymember, KIF1A, displayed nopreference for acetylated microtubulesin COS-7 cells.By biasing protein association witha particular subset of microtubules,acetylation allows for subpopulationsof microtubules to act ascompartments along which specificcargoes can find each other, and befound in return. In a sense, thesemicrotubule compartments can bethought of as cellular pubs that attracta specific cargo crowd for mingling.Microtubule acetylation is alsoprobably involved in the regulation ofcell migration both in fibroblasts [16]and neurons [17]. It is attractive tospeculate that polarization of movingcells requires kinesin-dependentrecruitment of selective cargoes to theleading edge of migrating cells.Additional investigation is necessaryto determine whether this selectivemotor recruitment applies to othermicrotubule modifications and othermotor proteins. It is possible that atleast some other microtubule motorshave a higher affinity for eithera specific tubulin isoform or a particularpost-translational modification, similarto the preferential recruitment ofkinesin-1 to acetylated microtubules.Such selectivity could create multiplemicrotubule compartments to recruitparticular cargoes — different pubs fordifferent crowds (Figure 1). Oncebound to microtubules, the cargo canundergo bidirectional transport tofacilitate its movement through thecrowded cytoplasm. Cargoes recruitedto the same subset of microtubules willinteract with much higher efficiency,thus promoting exchange of moleculesbetween particular cell compartments.If this simple model is correct, itindicates that, in addition to their roleas tracks for long-distance transport,microtubules serve an important role asscaffolds for the organization andcompartmentalization of the otherwiserandomly distributed cellularcomponents.References1. Westermann, S., and Weber, K. (2003).Post-translational modifications regulatemicrotubule function. Nat. Rev. Mol. Cell Biol.4, 938–947.2. Liao, G., and Gundersen, G.G. (1998). Kinesin isa candidate for cross-bridging microtubulesand intermediate filaments. Selective binding ofkinesin to detyrosinated tubulin and vimentin.J. Biol. Chem. 273, 9797–9803.3. Reed, N.A., Cai, D., Blasius, T.L., Jih, G.T.,Meyhofer, E., Gaertig, J., and Verhey, K.J.(2006). Microtubule acetylation promoteskinesin-1 binding and transport. Curr. Biol. 16,2166–2172.4. Dompierre, J.P., Godin, J.D., Charrin, B.C.,Cordelieres, F.P., King, S.J., Humbert, S., andSaudou, F. (2007). Histone deacetylase 6inhibition compensates for the transport deficitin Huntington’s disease by increasing tubulinacetylation. J. Neurosci. 27, 3571–3583.5. Konishi, Y., and Setou, M. (2009). Tubulintyrosination navigates the kinesin-1 motordomain to axons. Nat. Neurosci. 12, 559–567.6. Cai, D., McEwen, D.P., Martens, J.R.,Meyhofer, E., and Verhey, K.J. (2009). Singlemolecule imaging reveals differences inmicrotubule track selection between Kinesinmotors. PLoS Biol. 7, e1000216.7. Hammond, J.W., Huang, C.F., Kaech, S.,Jacobson, C., Banker, G., and Verhey, K.J.(2010). Posttranslational modifications oftubulin and the polarized transport of kinesin-1in neurons. Mol. Biol. Cell 21, 572–583.8. Friedman, J.R., Webster, B.M.,Mastronarde, D.N., Verhey, K.J., andVoeltz, G.K. (2010). ER sliding dynamics andER-mitochondrial contacts occur on acetylatedmicrotubules. J. Cell Biol. 190, 363–375.9. Voeltz, G.K., Rolls, M.M., and Rapoport, T.A.(2002). Structural organization of theendoplasmic reticulum. EMBO Rep. 3, 944–950.10. Terasaki, M., Chen, L.B., and Fujiwara, K.(1986). Microtubules and the endoplasmicreticulum are highly interdependent structures.J. Cell Biol. 103, 1557–1568.11. Waterman-Storer, C.M., and Salmon, E.D.(1998). Endoplasmic reticulum membranetubules are distributed by microtubules in livingcells using three distinct mechanisms. Curr.Biol. 8, 798–806.12. Allan, V., and Vale, R. (1994). Movement ofmembrane tubules along microtubules in vitro:evidence for specialised sites of motorattachment. J. Cell Sci. 107, 1885–1897.13. Wozniak, M.J., Bola, B., Brownhill, K.,Yang, Y.C., Levakova, V., and Allan, V.J. (2009).Role of kinesin-1 and cytoplasmic dynein inendoplasmic reticulum movement in VEROcells. J. Cell Sci. 122, 1979–1989.14. Nogales, E., Whittaker, M., Milligan, R.A., andDowning, K.H. (1999). High-resolution model ofthe microtubule. Cell 96, 79–88.15. Hoepfner, S., Severin, F., Cabezas, A.,Habermann, B., Runge, A., Gillooly, D.,Stenmark, H., and Zerial, M. (2005). Modulationof receptor recycling and degradation by theendosomal kinesin KIF16B. Cell 121, 437–450.16. Gundersen, G.G., and Bulinski, J.C. (1988).Selective stabilization of microtubules orientedtoward the direction of cell migration. Proc.Natl. Acad. Sci. USA 85, 5946–5950.17. Creppe, C., Malinouskaya, L., Volvert, M.L.,Gillard, M., Close, P., Malaise, O., Laguesse, S.,Cornez, I., Rahmouni, S., Ormenese, S., et al.(2009). Elongator controls the migration anddifferentiation of cortical neurons throughacetylation of alpha-tubulin. Cell 136, 551–564.Department of Cell and Molecular Biology,Northwestern University Feinberg Schoolof Medicine, Chicago, IL 60611, USA.*E-mail: vgelfand@northwestern.eduDOI: 10.1016/j.cub.2010.08.058Insect Vision: A Few Tricksto Regulate Flight AltitudeA recent study sheds new light on the visual cues used by Drosophilato regulate flight altitude. The striking similarity with previously identifiedsteering mechanisms provides a coherent basis for novel modelsof vision-based flight control in insects and robots.Dario Floreanoand Jean-Christophe ZuffereyInsects predominantly use vision tosteer, to regulate their flight speedand height, to avoid impendingobstacles, to chase moving targets,and to land on objects. Theirevolutionary success, ability to flyin complex environments, and theABCCurrent BiologyFigure 1. Visual regulation of altitude in Drosophila.Novel findings suggest that Drosophila regulate altitude (A) by aligning with static horizontaledges, (B) by increasing or decreasing lift in accordance with the vertical displacement of hori-zontal structure, and (C) by increasing lift in the presence of optic flow expansion in the ventralfield when flying at low altitude.Current Biology Vol 20 No 19R848relatively compact size of their brainsand bodies make flying insects notonly an appealing subject of researchfor biologists, but also a compellingsource of inspiration for computerscientists and engineers aiming atcreating vision-based flyingmachines [1].Many experimental studiesperformed so far on flying insectshave concentrated on visual cuesfor horizontal steering behaviors.Decades of observations ofinsects in arenas with controlledvisual stimulation have shown thatthey selectively respond to specificpatterns of retinal image motion(optic flow) to stabilize flight [2],regulate speed [3], and avoidcollisions [4]. However, little is knownabout the visual cues used to controlflight altitude. A recent computationalmodel [5], which was validated inexperiments with a miniaturehelicopter, predicts that insects mayregulate flight altitude by maintaininga constant angular speed of theventral optic flow — lower flightaltitude generates higher imagespeed in the ventral area of thecompound eyes.In contrast to this prediction,the novel experiments performedby Straw et al. [6], recentlypublished in Current Biology,suggest that Drosophila does notregulate altitude by monitoringimage speed in the ventral area.The authors used an advanced flightarena with computer-controlledspeed and direction of imagesprojected on the ground and walls.In a first series of experiments, theycancelled the natural motion of theground image caused by the insectflight and imposed a controlled setof ventral optic-flow speeds anddirections. Because insects didnot react to this optical stimulationby changing altitude, the authorsruled out the hypothesis thatventral optic flow is used tomaintain altitude andsearched for alternative ways inwhich Drosophila could regulatealtitude.In the first set of experiments,Straw et al. [6] showed that insectsroughly align their flight altitudewith the height of horizontal edgesthat appear near the eye equator,independently of the presence,speed, or direction of a ventral image.They also showed that insectschange flight altitude in order tomaintain alignment with verticallymoving horizontal edges (Figure 1A).This behavior is remarkably similarto previously identified behaviors ofhorizontal stabilization [7] andtracking of vertical edges [8],suggesting the duplication or useof the same neuronal circuitry forhorizontal steering and altituderegulation.In a second set of experiments,the authors showed that insectsincreased altitude when presentedwith lateral, upward movinghorizontal gratings and decreasedaltitude when presented withdownward moving gratings(Figure 1B). This behavior, whichcannot be explained by edgeDispatchR849alignment, could be mediatedby a separate mechanism tocompensate for unintended altitudechanges — dropping altitude wouldgenerate coherent upward motionof the image and thus triggerincreased lift. Once again, thisbehavior is reminiscent of the fly’soptomotor response to wide-fieldhorizontal shifts of the visual scenein order to compensate forunintended deviations from straightflight [9,10].In a third set of experiments, theyshowed that insects are alsosensitive to optic flow on the ventralarea, but only when the optic flowcorresponded to a pattern of radialexpansion centered under the insectat a height of less than 15 cm(Figure 1C). This behavior, whichcould serve as emergency collisionavoidance, is analogous to thewell-documented behavior of steeringaway from areas of expandingfields when flying on a horizontalplane [2].These results not only provide anovel explanation for flight altituderegulation, but also suggest thatinsects may use the same fewsensory-motor reflexes to controlflight in the three dimensions. Thishypothesis is very appealingbecause it provides the basis forthe formulation of a novel, coherenttheory of vision-based flightregulation that abstracts fromthe division between flight in thehorizontal and vertical dimensions.Such a theory could also generatenew predictions about the functionand architecture of the neuralcircuitries mapping opticalstimulation of the compoundeyes into motor control anddrive novel experiments to elucidatethe behavioral, neuronal, andgenetic basis of vision-basedflight control.Nonetheless, this study raisesa few questions. For example, it isnot clear to what extent the findingsapply also to other insect species.Experimental evidence indicates thathoneybees do regulate their ventraloptic flow, which makes them reactto varying ground speeds bychanging their altitude [11], aspredicted by the computationalmodel of Franceschini et al. [5].Furthermore, there seems to bea precise correlation between themagnitude of the ventral optic flowand the altitude of honeybeesduring landing [12]. Finally, it is notclear to what extent horizontal edgesare present in the natural habitat ofthese insects, at what distance theymust be to be used by the animal,and what happens to altituderegulation when no such edgesare present.The work of Straw et al. [6] alsoshows the increasing relevance ofcomputational models developedand tested on robots in order tounderstand biological principlesof behavioral systems. Althoughthe model of ventral optic flowregulation [5] was not confirmed byexperimental observations of thisstudy (notwithstanding the caveatsmentioned above), it did provide aprecise working hypothesis thatmotivated this novel study. In thefuture, robotics computational modelscould also be useful for preciselyformulating, refining, and validatingin an artificial behavioral system thenew mechanisms suggested byStraw et al. [6].Finally, these novel findings canalso guide the development ofnovel control strategies andoptoelectronic devices for miniaturerobots autonomously flying in urbanenvironments, in buildings, or inforests. Although engineers andcomputer scientists havesuccessfully used ventral optic flowto regulate altitude both insimulated [13] and real flying robots[14–17], those solutions assume thepresence of detectable texture inthe ventral area of the robot, whichin reality is not always the case.Horizontal contrast, which is oftenprominent in built environments andforests, could replace or complementother strategies for altitude control.The capability and need of detectinghorizontal contrasts near theequator line of the eyes may alsoaffect the design of artificialcompound eyes, which areattracting growing interest in theengineering community [18–20]because they could offer a fieldof view, size, and response speedthat is better than conventionalsingle-aperture cameras formotion-related tasks.References1. Floreano, D., Zufferey, J.-C., Srinivasan, M.V.,and Ellington, C. (2009). Flying Insects andRobots (Berlin: Springer).2. Egelhaaf, M., and Borst, A. (1993). A look intothe cockpit of the fly: visual orientation,algorithms, and identified neurons. J. Neurosci.13, 4563–4574.3. Srinivasan, M., Lehrer, M., Kirchner, W., andZhang, S. (1991). Range perceptionthrough apparent image speed in freely-flying honeybees. Visual Neurosci. 6,519–535.4. Tammero, L., and Dickinson, M. (2002).Collision-avoidance and landing responsesare mediated by separate pathways inthe fruit fly. J. Exp. Biol. 205,2785–2798.5. Franceschini, N., Ruffier, F., and Serres, J.(2007). A Bio-inspired flying robot shedslight on insect piloting abilities. Curr. Biol. 17,1–7.6. Straw, A.D., Lee, S., and Dickinson, M.H.(2010). Visual control of altitude inflying Drosophila. Curr. Biol. 20,1550–1556.7. Buchner, E. (1976). Elementary movementdetectors in an insect visual system. Biol.Cybernet. 24, 85–101.8. Horn, E., and Wehner, R. (1975). Themechanism of pattern fixation in the walking fly,Drosophila Melanogaster. J. Comp. Physiol.101, 39–56.9. Go¨tz, K. (1975). The optomotor equilibrium ofthe Drosophila navigation system. J. Comp.Physiol. 99, 187–210.10. Srinivasan, M., Poteser, M., and Kral, K. (1999).Motion detection in insect orientationand navigation. Vision Res. 39,2749–2766.11. Portelli, G., Ruffier, F., and Franceschini, N.(2010). Honeybees change their height torestore their optic flow. J. Comp. Physiol. ANeuroethol. Sens. Neural. Behav. Physiol.196, 307–313.12. Srinivasan, M., Zhang, S., Chahl, J., Barth, E.,and Venkatesh, S. (2000). How honeybeesmake grazing landings on flat surfaces. Biol.Cybernet. 83, 171–183.13. Neumann, T., Huber, S., and Bu¨lthoff, H.H.(2001). Artificial systems as models in biologicalcybernetics. Behavioral Brain Sci. 24,1071–1072.14. Ruffier, F., and Franceschini, N. (2005). Opticflow regulation: the key to aircraft automaticguidance. Robotics Autonomous Systems 50,177–194.15. Barber, D.B., Griffiths, S.R., McLain, T.W.,and Beard, R.W. (2007). Autonomouslanding of miniature aerial vehicles.J. Aerosp. Comp. Inf. Commun. 4,770–784.16. Beyeler, A., Zufferey, J.-C., andFloreano, D. (2009). Vision-based controlof near-obstacle flight. Auton. Robots 27,201–219.17. Zufferey, J.-C., Beyeler, A., and Floreano, D.(2010). Autonomous flight at low altitudeusing light sensors and little computationalpower. Int. J. Micro. Air Veh. 2,107–117.18. Duparre´, J., Dannberg, P., Schreiber, P.,Bra¨uer, A., and Tu¨nnermann, A. (2005). Thincompound eye camera. Appl. Optics 44,2949–2956.19. Radtke, D., Duparre´, J., Zeitner, U., andTu¨nnermann, A. (2007). Laser lithographicfabrication and characterization of a sphericalartificial compound eye. Opt. Exp. 15,3067–3077.20. Jeong, K.-H., Kim, J., and Lee, L.P. (2006).Biologically inspired artificial compound eyes.Science 312, 557–561.Laboratory of Intelligent Systems,Ecole Polytechnique Federale de Lausanne,CH-1015 Switzerland.E-mail: dario.floreano@epfl.chDOI: 10.1016/j.cub.2010.08.022

Insect Vision: A Few Tricks to Regulate Flight Altitude

Elsevier - Publisher Connector 

Insect Vision: A Few Tricks to Regulate Flight Altitude 

Dispatch
R847binding. Furthermore, as acetylation
occurs only after microtubule
polymerization, the enzyme
responsible for this modification
should probably localize to the
microtubule lumen.
The preference of ER sliding for
acetylated microtubules may indicate
a functional difference between this
type of ER motility and that mediated
by the tip attachment complex.
Intermembrane contacts are important
for many functions of the ER and
other membranous compartments [9].
The authors’ results led them to
hypothesize that the sliding
mechanism may be used as a way
for ER tubules to find and contact other
organelles along a subpopulation
of microtubules.
To explore this possibility, Friedman
et al. [8] tracked the movements of two
other organelles, mitochondria and
endosomes, with respect to both ER
and acetylated microtubules. A
majority of both organelles remained
in persistent contact with the ER.
However, only mitochondria appeared
to also localize preferentially to
acetylated microtubules, suggesting
that ER contacts with mitochondria,
but not endosomes, are enriched along
acetylated microtubules. Consistent
with this finding is the fact that both ER
and mitochondria are cargoes of
kinesin-1, while endosomes are moved
by KIF16B, a member of the kinesin-3
family [15]. Further, work byCai et al. [6]
showed that another kinesin-3 family
member, KIF1A, displayed no
preference for acetylated microtubules
in COS-7 cells.
By biasing protein association with
a particular subset of microtubules,
acetylation allows for subpopulations
of microtubules to act as
compartments along which specific
cargoes can find each other, and be
found in return. In a sense, these
microtubule compartments can be
thought of as cellular pubs that attract
a specific cargo crowd for mingling.
Microtubule acetylation is also
probably involved in the regulation of
cell migration both in fibroblasts [16]
and neurons [17]. It is attractive to
speculate that polarization of moving
cells requires kinesin-dependent
recruitment of selective cargoes to the
leading edge of migrating cells.
Additional investigation is necessary
to determine whether this selective
motor recruitment applies to other
microtubule modifications and othermotor proteins. It is possible that at
least some other microtubule motors
have a higher affinity for either
a specific tubulin isoform or a particular
post-translational modification, similar
to the preferential recruitment of
kinesin-1 to acetylated microtubules.
Such selectivity could create multiple
microtubule compartments to recruit
particular cargoes — different pubs for
different crowds (Figure 1). Once
bound to microtubules, the cargo can
undergo bidirectional transport to
facilitate its movement through the
crowded cytoplasm. Cargoes recruited
to the same subset of microtubules will
interact with much higher efficiency,
thus promoting exchange of molecules
between particular cell compartments.
If this simple model is correct, it
indicates that, in addition to their role
as tracks for long-distance transport,
microtubules serve an important role as
scaffolds for the organization and
compartmentalization of the otherwise
randomly distributed cellular
components.
References
1. Westermann, S., and Weber, K. (2003).
Post-translational modifications regulate
microtubule function. Nat. Rev. Mol. Cell Biol.
4, 938–947.
2. Liao, G., and Gundersen, G.G. (1998). Kinesin is
a candidate for cross-bridging microtubules
and intermediate filaments. Selective binding of
kinesin to detyrosinated tubulin and vimentin.
J. Biol. Chem. 273, 9797–9803.
3. Reed, N.A., Cai, D., Blasius, T.L., Jih, G.T.,
Meyhofer, E., Gaertig, J., and Verhey, K.J.
(2006). Microtubule acetylation promotes
kinesin-1 binding and transport. Curr. Biol. 16,
2166–2172.
4. Dompierre, J.P., Godin, J.D., Charrin, B.C.,
Cordelieres, F.P., King, S.J., Humbert, S., and
Saudou, F. (2007). Histone deacetylase 6
inhibition compensates for the transport deficit
in Huntington’s disease by increasing tubulin
acetylation. J. Neurosci. 27, 3571–3583.
5. Konishi, Y., and Setou, M. (2009). Tubulin
tyrosination navigates the kinesin-1 motor
domain to axons. Nat. Neurosci. 12, 559–567.6. Cai, D., McEwen, D.P., Martens, J.R.,
Meyhofer, E., and Verhey, K.J. (2009). Single
molecule imaging reveals differences in
microtubule track selection between Kinesin
motors. PLoS Biol. 7, e1000216.
7. Hammond, J.W., Huang, C.F., Kaech, S.,
Jacobson, C., Banker, G., and Verhey, K.J.
(2010). Posttranslational modifications of
tubulin and the polarized transport of kinesin-1
in neurons. Mol. Biol. Cell 21, 572–583.
8. Friedman, J.R., Webster, B.M.,
Mastronarde, D.N., Verhey, K.J., and
Voeltz, G.K. (2010). ER sliding dynamics and
ER-mitochondrial contacts occur on acetylated
microtubules. J. Cell Biol. 190, 363–375.
9. Voeltz, G.K., Rolls, M.M., and Rapoport, T.A.
(2002). Structural organization of the
endoplasmic reticulum. EMBO Rep. 3, 944–950.
10. Terasaki, M., Chen, L.B., and Fujiwara, K.
(1986). Microtubules and the endoplasmic
reticulum are highly interdependent structures.
J. Cell Biol. 103, 1557–1568.
11. Waterman-Storer, C.M., and Salmon, E.D.
(1998). Endoplasmic reticulum membrane
tubules are distributed by microtubules in living
cells using three distinct mechanisms. Curr.
Biol. 8, 798–806.
12. Allan, V., and Vale, R. (1994). Movement of
membrane tubules along microtubules in vitro:
evidence for specialised sites of motor
attachment. J. Cell Sci. 107, 1885–1897.
13. Wozniak, M.J., Bola, B., Brownhill, K.,
Yang, Y.C., Levakova, V., and Allan, V.J. (2009).
Role of kinesin-1 and cytoplasmic dynein in
endoplasmic reticulum movement in VERO
cells. J. Cell Sci. 122, 1979–1989.
14. Nogales, E., Whittaker, M., Milligan, R.A., and
Downing, K.H. (1999). High-resolution model of
the microtubule. Cell 96, 79–88.
15. Hoepfner, S., Severin, F., Cabezas, A.,
Habermann, B., Runge, A., Gillooly, D.,
Stenmark, H., and Zerial, M. (2005). Modulation
of receptor recycling and degradation by the
endosomal kinesin KIF16B. Cell 121, 437–450.
16. Gundersen, G.G., and Bulinski, J.C. (1988).
Selective stabilization of microtubules oriented
toward the direction of cell migration. Proc.
Natl. Acad. Sci. USA 85, 5946–5950.
17. Creppe, C., Malinouskaya, L., Volvert, M.L.,
Gillard, M., Close, P., Malaise, O., Laguesse, S.,
Cornez, I., Rahmouni, S., Ormenese, S., et al.
(2009). Elongator controls the migration and
differentiation of cortical neurons through
acetylation of alpha-tubulin. Cell 136, 551–564.Department of Cell and Molecular Biology,
Northwestern University Feinberg School
of Medicine, Chicago, IL 60611, USA.
*E-mail: vgelfand@northwestern.edu
DOI: 10.1016/j.cub.2010.08.058Insect Vision: A Few Tricks
to Regulate Flight Altitude
A recent study sheds new light on the visual cues used by Drosophila
to regulate flight altitude. The striking similarity with previously identified
steering mechanisms provides a coherent basis for novel models
of vision-based flight control in insects and robots.Dario Floreano
and Jean-Christophe Zufferey
Insects predominantly use vision to
steer, to regulate their flight speedand height, to avoid impending
obstacles, to chase moving targets,
and to land on objects. Their
evolutionary success, ability to fly
in complex environments, and the
AB
C
Current Biology
Figure 1. Visual regulation of altitude in Drosophila.
Novel findings suggest that Drosophila regulate altitude (A) by aligning with static horizontal
edges, (B) by increasing or decreasing lift in accordance with the vertical displacement of hori-
zontal structure, and (C) by increasing lift in the presence of optic flow expansion in the ventral
field when flying at low altitude.
Current Biology Vol 20 No 19
R848relatively compact size of their brains
and bodies make flying insects not
only an appealing subject of research
for biologists, but also a compelling
source of inspiration for computer
scientists and engineers aiming at
creating vision-based flying
machines [1].
Many experimental studies
performed so far on flying insectshave concentrated on visual cues
for horizontal steering behaviors.
Decades of observations of
insects in arenas with controlled
visual stimulation have shown that
they selectively respond to specific
patterns of retinal image motion
(optic flow) to stabilize flight [2],
regulate speed [3], and avoid
collisions [4]. However, little is knownabout the visual cues used to control
flight altitude. A recent computational
model [5], which was validated in
experiments with a miniature
helicopter, predicts that insects may
regulate flight altitude by maintaining
a constant angular speed of the
ventral optic flow — lower flight
altitude generates higher image
speed in the ventral area of the
compound eyes.
In contrast to this prediction,
the novel experiments performed
by Straw et al. [6], recently
published in Current Biology,
suggest that Drosophila does not
regulate altitude by monitoring
image speed in the ventral area.
The authors used an advanced flight
arena with computer-controlled
speed and direction of images
projected on the ground and walls.
In a first series of experiments, they
cancelled the natural motion of the
ground image caused by the insect
flight and imposed a controlled set
of ventral optic-flow speeds and
directions. Because insects did
not react to this optical stimulation
by changing altitude, the authors
ruled out the hypothesis that
ventral optic flow is used to
maintain altitude and
searched for alternative ways in
which Drosophila could regulate
altitude.
In the first set of experiments,
Straw et al. [6] showed that insects
roughly align their flight altitude
with the height of horizontal edges
that appear near the eye equator,
independently of the presence,
speed, or direction of a ventral image.
They also showed that insects
change flight altitude in order to
maintain alignment with vertically
moving horizontal edges (Figure 1A).
This behavior is remarkably similar
to previously identified behaviors of
horizontal stabilization [7] and
tracking of vertical edges [8],
suggesting the duplication or use
of the same neuronal circuitry for
horizontal steering and altitude
regulation.
In a second set of experiments,
the authors showed that insects
increased altitude when presented
with lateral, upward moving
horizontal gratings and decreased
altitude when presented with
downward moving gratings
(Figure 1B). This behavior, which
cannot be explained by edge
Dispatch
R849alignment, could be mediated
by a separate mechanism to
compensate for unintended altitude
changes — dropping altitude would
generate coherent upward motion
of the image and thus trigger
increased lift. Once again, this
behavior is reminiscent of the fly’s
optomotor response to wide-field
horizontal shifts of the visual scene
in order to compensate for
unintended deviations from straight
flight [9,10].
In a third set of experiments, they
showed that insects are also
sensitive to optic flow on the ventral
area, but only when the optic flow
corresponded to a pattern of radial
expansion centered under the insect
at a height of less than 15 cm
(Figure 1C). This behavior, which
could serve as emergency collision
avoidance, is analogous to the
well-documented behavior of steering
away from areas of expanding
fields when flying on a horizontal
plane [2].
These results not only provide a
novel explanation for flight altitude
regulation, but also suggest that
insects may use the same few
sensory-motor reflexes to control
flight in the three dimensions. This
hypothesis is very appealing
because it provides the basis for
the formulation of a novel, coherent
theory of vision-based flight
regulation that abstracts from
the division between flight in the
horizontal and vertical dimensions.
Such a theory could also generate
new predictions about the function
and architecture of the neural
circuitries mapping optical
stimulation of the compound
eyes into motor control and
drive novel experiments to elucidate
the behavioral, neuronal, and
genetic basis of vision-based
flight control.
Nonetheless, this study raises
a few questions. For example, it is
not clear to what extent the findings
apply also to other insect species.
Experimental evidence indicates that
honeybees do regulate their ventral
optic flow, which makes them react
to varying ground speeds by
changing their altitude [11], as
predicted by the computational
model of Franceschini et al. [5].
Furthermore, there seems to be
a precise correlation between the
magnitude of the ventral optic flowand the altitude of honeybees
during landing [12]. Finally, it is not
clear to what extent horizontal edges
are present in the natural habitat of
these insects, at what distance they
must be to be used by the animal,
and what happens to altitude
regulation when no such edges
are present.
The work of Straw et al. [6] also
shows the increasing relevance of
computational models developed
and tested on robots in order to
understand biological principles
of behavioral systems. Although
the model of ventral optic flow
regulation [5] was not confirmed by
experimental observations of this
study (notwithstanding the caveats
mentioned above), it did provide a
precise working hypothesis that
motivated this novel study. In the
future, robotics computational models
could also be useful for precisely
formulating, refining, and validating
in an artificial behavioral system the
new mechanisms suggested by
Straw et al. [6].
Finally, these novel findings can
also guide the development of
novel control strategies and
optoelectronic devices for miniature
robots autonomously flying in urban
environments, in buildings, or in
forests. Although engineers and
computer scientists have
successfully used ventral optic flow
to regulate altitude both in
simulated [13] and real flying robots
[14–17], those solutions assume the
presence of detectable texture in
the ventral area of the robot, which
in reality is not always the case.
Horizontal contrast, which is often
prominent in built environments and
forests, could replace or complement
other strategies for altitude control.
The capability and need of detecting
horizontal contrasts near the
equator line of the eyes may also
affect the design of artificial
compound eyes, which are
attracting growing interest in the
engineering community [18–20]
because they could offer a field
of view, size, and response speed
that is better than conventional
single-aperture cameras for
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E-mail: dario.floreano@epfl.chDOI: 10.1016/j.cub.2010.08.022


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Insect Vision: A Few Tricks to Regulate Flight Altitude

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