Visual control of prey-capture flight in dragonfliesRobert M Olberg

Available online at www.sciencedirect.com

Interacting with a moving object poses a computational

problem for an animal’s nervous system. This problem has

been elegantly solved by the dragonfly, a formidable visual

predator on flying insects. The dragonfly computes an

interception flight trajectory and steers to maintain it during its

prey-pursuit flight. This review summarizes current knowledge

about pursuit behavior and neurons thought to control

interception in the dragonfly. When understood, this system

has the potential for explaining how a small group of neurons

can control complex interactions with moving objects.

Address

Department of Biological Sciences, Union College, 807 Union Street,

Schenectady, NY 12308, USA

Corresponding author: Olberg, Robert M (olbergr@union.edu)

Current Opinion in Neurobiology 2012, 22:267–271

This review comes from a themed issue on

Neuroethology

Edited by Michael Dickinson and Cynthia Moss

Available online 21st December 2011

0959-4388/$ – see front matter

# 2011 Elsevier Ltd. All rights reserved.

DOI 10.1016/j.conb.2011.11.015

IntroductionInteracting with a moving object poses a computational

problem for an animal’s nervous system. Whether the

animal is catching a ball, a conspecific or a prey item, it

must predict the object’s future location to compensate

for the time required to process sensory information and

move to the point of interception. The dragonfly is a

superb example of an animal that captures rapidly moving

prey. In this review I will summarize what is known about

capture strategies, focusing especially on the dragonfly, its

interception behavior and its nervous system.

Dragonfly eyes and vision

With as many as 30,000 ommatidea [1] the dragonfly

compound eye is among the largest of insect eyes. The

eye covers the majority of the head (Figure 1a), so that the

dragonfly’s visual field is nearly a complete sphere. A

major regional specialization of the eye is the presence of

a ‘dorsal acute zone’ a region of the eye with larger facets

and more closely aligned optical axes [1,2]. The dorsal

acute zone forms a crescent of relatively high resolution

about 558 above the horizon, and projecting at right angles

to visual midline down toward the horizon on each side of

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the head. Behavioral evidence suggests that this region is

important for detecting [3] and pursuing [4] flying-insect

prey. The dorsal acute zone in the dragonfly Sympetrum is

exclusively sensitive to short wavelengths of light (blue

and UV) [5], a regional specialization for foraging against

blue sky, whereas at least five spectral types of photo-

receptors are present in the ventral eye [6] (see review by

Stavenga [7]). Finally, physiological [8], anatomical [9],

and behavioral evidence [10,11] indicate that the dragon-

fly eye is polarization sensitive. Whether polarized light is

important for prey pursuit is not known.

Optic lobes

There have been many excellent studies of the peripheral

optic lobes of dragonflies, both anatomical [12–14] and

physiological [6,8,9,15–19]. However, this review of the

neural basis of prey interception will begin with the third

optic neuropil, the lobula complex. O’Carroll [20�] first

described neurons in the lobula complex that were exqui-

sitely sensitive (and usually directionally selective) to

small-target (1–28) motion but not at all to longer bars

or gratings. He suggested that these neurons were likely

to contribute to the detection of prey or other dragonflies.

In further studies the lobular neurons were termed Small

Target Motion Detectors (STMDs). One of these,

CSTMD1, was identified anatomically by Geurten

et al. [21] who explored the lateral inhibitory connections

that underlie its small target selectivity. Bolzon et al. [22]

presented evidence that the two contralateral homolog

CSTMD1s inhibit one another, providing long-range

inhibition in addition to the local inhibitory connections.

They suggested that such interocular inhibition could

support attention to one target in the presence of poten-

tially distracting targets. A more detailed treatment of the

target-selective neurons in the lobula complex can be

found in the Nordstrom review in this volume [23].

The STMDs of the lobula are likely to provide indirect

input to another set of identified neurons, called Target-

Selective Descending Neurons (TSDNs) [24–26], which

transmit target motion information from the protocereb-

rum down the ventral nerve cord (VNC) to the thoracic

ganglia. In the Aeshnid dragonflies in which they were

identified, TSDN axons run through the dorsal VNC,

passing through the abdominal ganglia in either the

median dorsal tract (MDT) or the dorsal intermediate

tract (DIT), and they are named accordingly. Unlike

STMDs, each of the TSDNs is completely silent unless

the dragonfly is presented with a target of appropriate size

within its receptive field and in its preferred direction.

TSDNs vary in their preferred target-size preference, and

all show very rapid and long lasting habituation to target

Current Opinion in Neurobiology 2012, 22:267–271

268 Neuroethology

Figure 1

(b) (c) (d)

(f) (g)(e)

(a)

Current Opinion in Neurobiology

Dragonfly interception flights guided by compound eyes. (a) Perched

dragonfly Pachydiplax longipennis showing large compound eyes and

outstretched wings. Photo by Tom D. Schultz. (b–g) Digitized high-

speed video records (500 frames/s) of six flights of Erythemis

simplicicollis to a 2 mm white bead moved on a fine monofilament. Open

circles mark bead locations at 2 ms intervals with larger open circles

every 10 frames (20 ms). First open circle marks bead location at takeoff.

Filled diamonds indicate center of dragonfly head with large filled circle

every 20 ms. Gray lines indicate the length and position of dragonfly

body (no lines in d, e, and g, because animal viewed head-on). Plus signs

at a–c and f indicate position of head and bead at capture. Calibration

bars = 2 cm. (b–d) Straight-line interception course when bead moves

along a linear trajectory. (e–g) Turns in response to changes in bead

direction.

Reproduced with permission from Ref. [4].

motion repeated along the same trajectory. The TSDNs

show complex responses to color contrast over a wide

color spectrum, leading Horridge [27] to conclude that

that they receive (indirect) inputs from a variety of re-

ceptor types, but that they do not signal object color.

When stimulated intracellularly, TSDNs elicit small

movements of the wings that we interpret as steering

adjustments. The receptive fields of all of these neurons

are located in the dorso-frontal visual field, and include

some of the dorsal acute zone. As will be described below,

this is the region of prey fixation during pursuit.

Current Opinion in Neurobiology 2012, 22:267–271

Prey capture behaviorDragonflies forage on flying insects. They approach their

prey from below, tipping upward at the final moment of

approach to secure the prey with their outstretched legs.

Some species of dragonflies (‘perchers’) are sit-and-wait

predators, perching on the ground or on vegetation and

periodically taking off to intercept small insects as they fly

by. Others (‘hawkers’) remain in flight continuously

throughout the day, periodically swooping up to grab

insects passing overhead [28�]. Prey-capture flights are

highly accurate; reported capture success rates range from

76% [29] to as high as 97% [30].

Olberg et al. [30] studied prey capture in Libellulid

dragonflies (perchers) in the field. This study was fol-

lowed by a high-speed video study of dragonflies ‘captur-

ing’ tethered beads in an outdoor arena [4]. The

movements of the ‘prey,’ a bead on a fine nylon or

tungsten line, were restricted to a plane containing the

dragonfly and normal to the camera axis, resulting in

flights that were mostly in two dimensions, simplifying

analysis.

Before taking off after a flying object, the dragonfly

estimates its distance and thus its absolute size. We know

this, because the dragonfly only takes off after objects in

an appropriate absolute size range, implying that it is able

to assess distance [31]. How this distance estimation is

done is not known, but the most likely explanation is the

use of motion parallax information from a head bob [31–33] that precedes flight. When a target passes by over-

head, the dragonfly’s head rocks up with a large transla-

tional component in addition to the rotation. As the head

moves, images of nearby objects move farther on the

retina than farther objects, a potential source of distance

information. Motion parallax is used for distance esti-

mation in grasshoppers [34–36] and for figure/ground

discrimination in honeybees [37].

Interception

After taking off, how does the dragonfly approach its prey?

Collett and Land [38�] described two alternative strat-

egies that might be employed in insect chases, ‘tracking’

versus ‘interception’. In tracking, the pursuer aims

directly at the perceived location of the target, usually

resulting in a spiraling approach. In interception the

pursuer flies toward a point in front of the target, resulting

in a relatively straight approach to the point of contact. In

their study of hoverfly chases, Collett and Land [38�]found that the male pursuit of females is an interception

flight; the male often takes off in an entirely different

direction from the direction of the female when first

detected, only to intercept her as her course intersects

his own. They proposed that the males use a special

algorithm that applies only to intercepting female hover-

flies, because it is based on the known size and flight

speed of the female.

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Visual control of prey-capture flight in dragonflies Olberg 269

Dragonflies chase prey of highly variable size and flight

speed. Nevertheless, digitized flight tracks from free

flying dragonflies in the field [30] and in an outdoor flight

arena [4] reveal that the dragonfly steers an interception

course to capture its prey, that is, the trajectory is aimed

directly toward the point of contact rather than toward the

prey (Figure 1b–d). The interception flight is under

continuous visual control, so that a change in the prey’s

flight speed or direction elicits a change in the dragonfly’s

flight course (Figure 1e–g), with a remarkably short

latency of about 30 ms [4].

Interception trajectories have been documented in a wide

variety of animals in addition to hoverflies and dragon-

flies, including teleost fish catching food items [39], bats

catching flying insects [40], dogs catching Frisbees [41],

and humans catching baseballs [42] or walking to targets

in a virtual environment [43].

What neural computations underlie the ability of these

animals to intercept moving targets? They could be using

a simple tactic, known as the Constant Bearing Decreas-

ing Range (CBDR) strategy. This stems from a very old

nautical discovery that if another ship remains at the same

bearing and is getting closer, it is on a collision course with

the observing ship. CBDR reduces the complexity of the

interception problem, because the pursuer does not need

to know the absolute size, velocity, or distance of the

target; the pursuer simply needs to steer to maintain its

target at a constant bearing. The CBDR interception

strategy has been formalized in a guidance law known

as proportional navigation. In proportional navigation the

pursuer maintains a constant line-of-sight angle to the

target by applying rotational acceleration in the direction

of, and in proportion to, the line-of-sight angular velocity

of the target [44]. It is important to recognize that the

existence of a constant bearing from pursuer to target

does not necessarily imply a proportional navigation

strategy. However, proportional navigation is a parsimo-

nious way to achieve constant bearings.

The dragonfly appears to employ a constant bearing

strategy to intercept its prey, but whether its turning

responses reflect a proportional navigation mechanism

has not yet been determined. If so, the dragonfly only

needs to know the angular velocity of the prey image and

then generate proportional compensatory turning [4,30]

based on that information. The TSDNs in the dragonfly’s

nerve cord are excellent candidates to mediate such an

interception strategy. They are the largest, fastest axons

in the cord. They show directional responses to small-

object movement. They have receptive fields in the

direction that prey are fixated. Their responses increase

with object angular speed. And their activity drives steer-

ing movements of the wings. Interestingly two TSDNs

appear to predict future target location, with each spike

containing more information about future than present

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location [45��], a predictive property that might allow

them to compensate for visual latency.

It is possible that dragonflies could employ a slightly

different interception strategy, one described for foraging

bats [40]. Rather than maintaining a constant line-of-sight

bearing, bats appear to maintain a constant absolute angle

to their prey. This strategy has been shown to minimize

the time to interception of an erratically flying prey [40].

Maintaining a constant absolute angle also results in the

pursuer being stationary with respect to the background

from the viewpoint of the target. This lack of relative

motion results in ‘motion camouflage,’ and segments of

dragonfly chases have been analyzed that exhibit this

property [46].

Not all animals employ interception strategies. ‘Tracking’

strategies, where the pursuer heads directly toward the

target, have been described in free flying honeybees

pursuing target feed stations [47] and in several species

of male flies chasing females, other males or other small

targets [48,49,50��]. Tiger beetles show an open-loop

form of tracking, with short bouts of running toward their

prey punctuated by stops to reorient in the prey’s direc-

tion [51]. Interestingly, in response to a more slowly

moving, artificial prey item, the tiger beetle behavior

switches to continuous, closed-loop tracking. Both track-

ing and interception can be viewed as constant bearing

strategies, tracking being the special case in which the

bearing is held near 08 (straight ahead). Therefore pro-

portional navigation could result in either tracking or

interception scenarios.

Head movements

During the interception flight the dragonfly orients its

head so that the image of the prey falls within about 108 of

the intersection between the visual midline and the dorsal

acute zone [4]. This implies that the dragonfly is usually

not ‘looking’ in the direction of its flight path and rules out

a simple form of flight control in which the dragonfly flies

in the direction of its gaze. In addition, because the head

rotates to stabilize the prey image, the target image

displacement on the retina is probably much smaller than

it would be if the dragonfly were not fixating the prey.

Finally, since head orientation relative to the body is not

fixed, maintaining an interception course requires infor-

mation about head position. Head position information is

transmitted by a group of physiologically identified, mul-

timodal, descending neurons that show directionally se-

lective responses to rotation in various planes [52]. These

neurons could potentially be part of the neuronal circuitry

controlling the interception flight.

An unsolved problem in understanding target pursuit is

the conflict between the visual pathways signaling target

motion and those signaling wide-field motion that serve to

stabilize the eye in the visual environment. The problem

Current Opinion in Neurobiology 2012, 22:267–271

270 Neuroethology

is that any turn toward a target will be opposed by the

wide-field optomotor stabilization system. Nothing is

known about how these neural systems interact in the

dragonfly, but Trischler et al. have shown in free-flight

experiments with blowflies that the target-pursuit system

largely inhibits the optomotor response to a moving back-

ground [50��].

ConclusionsIn the dragonfly, eight pairs of descending interneurons

(TSDNs) are implicated as key elements in directing

aerial interceptions, and these interceptions are probably

based on flight corrections to maintain the prey at a

constant angle. Perhaps the best way to further our un-

derstanding of the role of the TSDNs in the behavior is to

record their activity while the behavior is playing out.

Work is underway in the Leonardo Lab (Janelia Farm,

HHMI) to do just that. A chronically implanted electrode

will record TSDN activity wirelessly in a freely flying

dragonfly outfitted with a small telemetry unit [53]. If this

attempt is successful it may be possible to reconstruct

precisely the visual input to the TSDNs during pursuit

and to infer the flight adjustments that result from their

activity, closing the loop from visual input to neuronal

activity to behavior.

AcknowledgementsI thank Andrea Worthington and the reviewers for helpful comments on themanuscript. This work was supported by the Air Force Office of ScientificResearch award FA9550-10-1-0472.

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