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  • Review Article
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Fly visual course control: behaviour, algorithms and circuits

Nature Reviews Neuroscience volume 15, pages 590–599 (2014)Cite this article

Subjects

Key Points

  • Fly visual behaviour is studied mostly in tethered flying or walking animals under open- or closed-loop conditions. In this way, three behaviours have been described: the optomotor response, the fixation response and the avoidance–landing response.

  • The optomotor response is elicited by rotation of a large-field visual panorama around the fly and consists of turning tendency that is syndirectional with the panorama. The fixation response describes the tendency of flies to keep a single black bar in front of them. In response to a lateral looming stimulus, flies rapidly turn away (the avoidance response). When the looming stimulus is in front of them, they perform a landing response.

  • On the basis of quantitative measurements of the stimulus–response relationships, algorithmic models were developed involving arrays of elementary motion detectors (EMDs) and elementary position detectors (EPDs) that cover the visual space and extract the local direction of motion and presence of an object. After appropriate spatial integration by large-field units, these models can accurately describe the respective behavioural response.

  • In search for the neural circuits, genetic targeting of individual cell types in the optic lobe identified lamina neurons L1 and L2 as the major input neurons for two parallel EMDs, one sensitive to moving brightness increments (ON-channel) and the other sensitive to brightness decrements (OFF-channel). T4 and T5 cells provide the directionally selective output of both EMDs, respectively, synapsing onto large-field tangential cells of the lobula plate, which control the optomotor response.

  • Further circuit elements of the EMD have been anatomically identified using serial sectioning electron microscopy. The function of these neurons is currently being tested in physiological experiments.

  • Blocking both T4 and T5 cells results in a complete loss of direction selectivity but leaves the position system largely intact. Thus, a circuit module representing the EPD must exist that is, at least partially, parallel to the EMD.

Abstract

Understanding how the brain controls behaviour is undisputedly one of the grand goals of neuroscience research, and the pursuit of this goal has a long tradition in insect neuroscience. However, appropriate techniques were lacking for a long time. Recent advances in genetic and recording techniques now allow the participation of identified neurons in the execution of specific behaviours to be interrogated. By focusing on fly visual course control, I highlight what has been learned about the neuronal circuit modules that control visual guidance in Drosophila melanogaster through the use of these techniques.

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Figure 1: Schematic of the fly's nervous system.
Figure 2: Visually driven behaviours and their algorithmic control circuits.
Figure 3: Cellular constituents of the optomotor response.
Figure 4: Neural control circuits underlying the fixation, optomotor and avoidance responses.

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Acknowledgements

T. Schilling provided unpublished data for figure 2. I thank her, A. Bahl, J. Haag and A. Leonhardt for helpful discussions and comments on the manuscript, C. Thalhammer for secretarial help and R. Schorner for art work.

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  1. Max Planck Institute of Neurobiology Systems and Computational Neuroscience, Am Klopferspitz 18, Martinsried, 82152, Germany

    Alexander Borst

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Glossary

Genetically encoded calcium indicators

Protein constructs, which are based on green fluorescent protein and a calcium-binding moiety, engineered to change their fluorescence upon increased calcium levels.

Closed-loop

A behavioural paradigm in which the animal's response is fed back onto the stimulus, such as in virtual reality.

Open-loop

A behavioural paradigm in which the animal's response is measured as a function of a stimulus completely defined by the experimenter, with no influence of the behavioural response on the stimulus.

Driver lines

Fly lines, each carrying a cell-specific enhancer in conjunction with a transcription factor such as Gal4 or LexA: when a fly line is crossed with a reporter line, a certain gene is expressed in the respective neurons.

Direction selectivity

A response property of a neuron describing its selectivity for the direction of visual motion.

Null direction

A certain direction of motion, usually opposite to the preferred direction, which inhibits a neuron maximally or excites it minimally.

Preferred direction

A certain direction of motion that excites a neuron maximally.

Halteres

Small, club-shaped appendices of the thorax modified from the hind wings. They beat in anti-phase to the wings when the fly is flying and function as gyroscopes, informing the insect about rotation of the body during flight.

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Borst, A. Fly visual course control: behaviour, algorithms and circuits. Nat Rev Neurosci 15, 590–599 (2014). https://doi.org/10.1038/nrn3799

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