The dragonfly is a swift and efficient hunter. Once it spots its prey,
it takes about half a second to swoop beneath an unsuspecting insect and
snatch it from the air. Scientists at the Howard Hughes Medical
Institute's Janelia Research Campus have used motion-capture techniques
to track the details of that chase, and found that a dragonfly's
movement is guided by internal models of its own body and the
anticipated movement of its prey. Similar internal models are used to
guide behavior in humans.
"This highlights the role that internal models play in letting these
creatures construct such a complex behavior," says Janelia group leader
Anthony Leonardo, who led the study. "It starts to reshape our view of
the neural underpinnings of this behavior." Leonardo, postdoctoral
fellows Matteo Mischiati and Huai-Ti Lin, and their colleagues published
the findings in the December 11, 2014, issue of the journal Nature.
"Until now, this type of complex control, which incorporates both
prediction and reaction, had been demonstrated only in vertebrates,"
writes Harvard University biologist Stacey A. Combes in an accompanying
News & Views perspective in Nature. "However, Mischiati et al. show
that dragonflies on the hunt perform internal calculations every bit as
complex as those of a ballet dancer."
Neuroscientists have learned a lot about how the nervous system
triggers actions in response to sensory information by studying simple
reflexive behaviors, such as how an animal escapes a predator. Leonardo
has been studying prey capture in dragonflies because he wants to know
whether the same stimulus-response loops that researchers have uncovered
in those systems also underlie more complex behaviors.
In humans, the simple act of reaching for an object demands
sophisticated information processing, Leonardo says. Just to pick up a
cup of coffee, the brain calls on a number of internal models. "You have
an internal model of how your arm works, how the joints are
articulated, of the cup and its mass. If the cup is filled with coffee,
you incorporate that," he explains. "Articulating a body and moving it
through space is a very complicated problem." Scientists had so far
thought of prey capture by insects as a straightforward system in which a
predator's movement is guided solely by the position its prey. "The
idea was the dragonfly roughly knows where the prey is relative to him,
and he tries to hold this angle constant as he moves toward the
interception point. This is the way guided missiles work and how people
catch footballs," Leonardo says. But there was reason to believe prey
capture was more complicated.
"You don't need a spectacularly complicated model to guess where the
prey will be a short time in the future," he says. "But how do you
maneuver your body to reach the point of contact?"
In search of a more complete picture, Leonardo and his team spent
several years devising a system that allows them to track a dragonfly's
body movements as it intercepts its prey. Their strategy is based on the
same motion-capture technology used to translate actors' movements into
computer animation: reflective markers are placed on different body
parts -- in this case, the head, body, and wings -- and a high-speed
video camera records flashes of light reflected from each marker as the
insect moves. Using the position of each flash of light, the scientists
can reconstruct an outline of the dragonfly as it flies (the accuracy of
the outline depends on the number of markers attached to the
dragonfly).
Leonardo and his colleagues recorded dragonflies' movements as they
chased after either a fruit fly or an artificial prey -- a bead
maneuvered by a pulley system -- whose movements the scientists could
precisely control. They focused on following the orientation of the
dragonfly's head and body. "That tells us what the dragonfly sees and
how its body moves," he explains.
When they analyzed their videos, it was clear that the dragonflies
were not simply responding to the movements of the prey. Instead, they
made structured turns that adjusted the orientation of their bodies --
even when their prey's trajectory did not change. "Those turns were
driven by the dragonfly's internal representation of its body and the
knowledge that it has to rotate its body and line it up to the prey's
flight path in a particular way," Leonardo says.
The dragonflies always aligned themselves so that they would
intercept their prey from below, reducing the risk of detection. "At the
end of the chase, the fly makes a basket out its legs and the prey
drops into it," Leonardo says.
Those shifts in orientation create a challenge for the predator. "The
dragonfly is making a lot of turns to line itself up. Those turns
create a lot of apparent prey motion. If the whole world is going to
spin, how can it possibly see its prey?" Leonardo asks. Surprisingly,
the scientists found that each dragonfly moved its head to keep the
image of its prey centered on the eye, despite the rotation of its own
body. The head movements happened too fast to be a reaction to visual
disturbances created by the rotation of the dragonfly's body, Leonardo
says. Instead, the head movements must be planned based on the insect's
predictions about how to stabilize the image of its prey.
Leonardo says the movements his team observed are so fine-tuned that
they keep the image of the prey fixed in the crosshairs of the
dragonfly's eyes -- their area of greatest acuity -- during the duration
of the chase. That allows the dragonfly to receive two channels of
information about its prey, Leonardo says. The angle between the head
and the body tracks the predicted movement of the prey, while the visual
system detects any unexpected movement when the prey strays from its
position in the crosshairs. "It gives the dragonfly a very elegant
combination of predicted model-driven control and the original reactive
control," he says.
Video: Dragonfly prey capture http://bcove me/jln0dlu8
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