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The role of direction-selective visual interneurons T4 and T5 in Drosophila orientation behavior

In order to safely move through the environment, visually-guided animals
use several types of visual cues for orientation. Optic flow provides faithful
information about ego-motion and can thus be used to maintain a straight
course. Additionally, local motion cues or landmarks indicate potentially
interesting targets or signal danger, triggering approach or avoidance, respectively.
The visual system must reliably and quickly evaluate these cues
and integrate this information in order to orchestrate behavior. The underlying
neuronal computations for this remain largely inaccessible in higher
organisms, such as in humans, but can be studied experimentally in more
simple model species. The fly Drosophila, for example, heavily relies on
such visual cues during its impressive flight maneuvers. Additionally, it is
genetically and physiologically accessible. Hence, it can be regarded as an
ideal model organism for exploring neuronal computations during visual
processing.

In my PhD studies, I have designed and built several autonomous virtual
reality setups to precisely measure visual behavior of walking flies. The
setups run in open-loop and in closed-loop configuration. In an open-loop
experiment, the visual stimulus is clearly defined and does not depend on
the behavioral response. Hence, it allows mapping of how specific features
of simple visual stimuli are translated into behavioral output, which can
guide the creation of computational models of visual processing. In closedloop
experiments, the behavioral response is fed back onto the visual stimulus,
which permits characterization of the behavior under more realistic
conditions and, thus, allows for testing of the predictive power of the computational
models.

In addition, Drosophila’s genetic toolbox provides various strategies for
targeting and silencing specific neuron types, which helps identify which
cells are needed for a specific behavior. We have focused on visual interneuron
types T4 and T5 and assessed their role in visual orientation behavior.
These neurons build up a retinotopic array and cover the whole visual field
of the fly. They constitute major output elements from the medulla and have
long been speculated to be involved in motion processing.
This cumulative thesis consists of three published studies: In the first
study, we silenced both T4 and T5 neurons together and found that such flies
were completely blind to any kind of motion. In particular, these flies could
not perform an optomotor response anymore, which means that they lost
their normally innate following responses to motion of large-field moving
patterns. This was an important finding as it ruled out the contribution
of another system for motion vision-based behaviors. However, these flies
were still able to fixate a black bar. We could show that this behavior is
mediated by a T4/T5-independent flicker detection circuitry which exists in
parallel to the motion system.

In the second study, T4 and T5 neurons were characterized via twophoton
imaging, revealing that these cells are directionally selective and
have very similar temporal and orientation tuning properties to directionselective
neurons in the lobula plate. T4 and T5 cells responded in a
contrast polarity-specific manner: T4 neurons responded selectively to ON
edge motion while T5 neurons responded only to OFF edge motion. When
we blocked T4 neurons, behavioral responses to moving ON edges were
more impaired than those to moving OFF edges and the opposite was true
for the T5 block. Hence, these findings confirmed that the contrast polarityspecific
visual motion pathways, which start at the level of L1 (ON) and L2
(OFF), are maintained within the medulla and that motion information is
computed twice independently within each of these pathways.
Finally, in the third study, we used the virtual reality setups to probe the
performance of an artificial microcircuit. The system was equipped with a
camera and spherical fisheye lens. Images were processed by an array of
Reichardt detectors whose outputs were integrated in a similar way to what
is found in the lobula plate of flies. We provided the system with several rotating
natural environments and found that the fly-inspired artificial system
could accurately predict the axes of rotation.

Identiferoai:union.ndltd.org:MUENCHEN/oai:edoc.ub.uni-muenchen.de:18047
Date27 February 2015
CreatorsBahl, Armin
PublisherLudwig-Maximilians-Universität München
Source SetsDigitale Hochschulschriften der LMU
Detected LanguageEnglish
TypeDissertation, NonPeerReviewed
Formatapplication/pdf
Relationhttp://edoc.ub.uni-muenchen.de/18047/

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