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Functional and developmental characterization of local motion sensing neurons in the fly visual system
Functional and developmental characterization of local motion sensing neurons in the fly visual system
Sighted animals use visual motion information to navigate in their environment, to search for food sources or mating partners and to avoid potentials predators. However, directional motion information is not explicitly represented in the photoreceptor signals, but rather needs to be extracted by postsynaptic circuits. For such a motion computation, different algorithmic models were proposed. The most prominent model multiplies the signal of two neighboring photoreceptors after one of them was temporally delayed. Fruit flies are well suited as a model organism to study the neuronal mechanisms underlying motion perception. With a low spatial but high temporal visual resolution, fruit flies are able to detect many different kinds of motion stimuli and perform a wide range of visually evoked behaviors. Thanks to the multitude of genetic tools optimized for Drosophila melanogaster, detailed manipulation of neuronal function can be performed on a molecular as well as on a cellular level. These tools allow to dissect the components of a neuronal circuit and investigate their respective function. In the visual system of flies exist neurons sensitive to wide field motion, which are important for the course control of flies. An open question remains the computation of upstream neurons detecting local motion. During my doctoral work I studied various aspects of the local motion sensing cells in the fly visual system: their functional properties, their importance for different behavioral tasks as well as their differentiation during development. In the first manuscript included in this thesis, we demonstrated that T4 and T5 cells are the elementary local motion sensing neurons of the fly. Calcium activity imaging of T4 and T5 cells revealed that four subtypes exist, each sensitive to motion along one of the four cardinal directions. Moreover, T4 cells responded specifically to light increments and T5 cells to light decrements. Blocking T4 neurons abolished the ON motion responses of postsynaptic lobula plate tangential cells. Accordingly, inactivating T5 cells inhibited the reaction of lobula plate tangential cells to OFF motion. We confirmed this effect by examining the turning behavior of walking flies with either T4 or T5 cells blocked. Flies without T4 output responded only to OFF edge motion, while flies with blocked T5 cells responded exclusively to ON edge motion. To investigate the functional role of the local motion sensing T4 and T5 cells, we studied the consequences of blocking these neurons and tested visual behavior. In the second manuscript, we described that inactivating T4 and T5 cells abolished the optomotor turning response of the flies. However, the motion blind flies were still able to orient towards a dark, vertical bar. Wedemonstrated that flies respond to the position of a bar independent of a motion cue. Therefore, we concluded that flies use positional as well as motion information to orient towards an attractive object. In the third manuscript, we further investigated the role of T4 and T5 cells in flight behavior and found these cells involved in the detection of expansion motion. Flight avoidance turns as well as landing responses of flies depend on functional T4 and T5 cells. These behaviors are evoked by expansion motion like a looming stimulus, which mimics an approaching predator or object. The importance of T4 and T5 cells for looming evoked behavior suggests, that these cells are not only connected to lobula plate tangential cells, which respond to rotatory wide-field motion, but are also presynaptic to looming sensitive neurons in the lobula plate. The last manuscript describes transcription factors important for the differentiation of T4 and T5 neurons. The morphology of all T4 and T5 subtypes is comparable; their dendrites are oriented opposite to the preferred direction of the cell and the axon terminals target one of the four lobula plate layers. Both the dendrites and the axon terminals are limited to only one layer of their respective neuropil. We found two postmitotic transcription factors expressed in the young T4 and T5 cells, SoxN and Sox102F, which regulate the common features of all subtypes. These transcription factors are crucial for the proper morphology of the T4 and T5 cells, as well as the function of the adult neurons.
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Schilling, Tabea
2019
English
Universitätsbibliothek der Ludwig-Maximilians-Universität München
Schilling, Tabea (2019): Functional and developmental characterization of local motion sensing neurons in the fly visual system. Dissertation, LMU München: Faculty of Biology
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Abstract

Sighted animals use visual motion information to navigate in their environment, to search for food sources or mating partners and to avoid potentials predators. However, directional motion information is not explicitly represented in the photoreceptor signals, but rather needs to be extracted by postsynaptic circuits. For such a motion computation, different algorithmic models were proposed. The most prominent model multiplies the signal of two neighboring photoreceptors after one of them was temporally delayed. Fruit flies are well suited as a model organism to study the neuronal mechanisms underlying motion perception. With a low spatial but high temporal visual resolution, fruit flies are able to detect many different kinds of motion stimuli and perform a wide range of visually evoked behaviors. Thanks to the multitude of genetic tools optimized for Drosophila melanogaster, detailed manipulation of neuronal function can be performed on a molecular as well as on a cellular level. These tools allow to dissect the components of a neuronal circuit and investigate their respective function. In the visual system of flies exist neurons sensitive to wide field motion, which are important for the course control of flies. An open question remains the computation of upstream neurons detecting local motion. During my doctoral work I studied various aspects of the local motion sensing cells in the fly visual system: their functional properties, their importance for different behavioral tasks as well as their differentiation during development. In the first manuscript included in this thesis, we demonstrated that T4 and T5 cells are the elementary local motion sensing neurons of the fly. Calcium activity imaging of T4 and T5 cells revealed that four subtypes exist, each sensitive to motion along one of the four cardinal directions. Moreover, T4 cells responded specifically to light increments and T5 cells to light decrements. Blocking T4 neurons abolished the ON motion responses of postsynaptic lobula plate tangential cells. Accordingly, inactivating T5 cells inhibited the reaction of lobula plate tangential cells to OFF motion. We confirmed this effect by examining the turning behavior of walking flies with either T4 or T5 cells blocked. Flies without T4 output responded only to OFF edge motion, while flies with blocked T5 cells responded exclusively to ON edge motion. To investigate the functional role of the local motion sensing T4 and T5 cells, we studied the consequences of blocking these neurons and tested visual behavior. In the second manuscript, we described that inactivating T4 and T5 cells abolished the optomotor turning response of the flies. However, the motion blind flies were still able to orient towards a dark, vertical bar. Wedemonstrated that flies respond to the position of a bar independent of a motion cue. Therefore, we concluded that flies use positional as well as motion information to orient towards an attractive object. In the third manuscript, we further investigated the role of T4 and T5 cells in flight behavior and found these cells involved in the detection of expansion motion. Flight avoidance turns as well as landing responses of flies depend on functional T4 and T5 cells. These behaviors are evoked by expansion motion like a looming stimulus, which mimics an approaching predator or object. The importance of T4 and T5 cells for looming evoked behavior suggests, that these cells are not only connected to lobula plate tangential cells, which respond to rotatory wide-field motion, but are also presynaptic to looming sensitive neurons in the lobula plate. The last manuscript describes transcription factors important for the differentiation of T4 and T5 neurons. The morphology of all T4 and T5 subtypes is comparable; their dendrites are oriented opposite to the preferred direction of the cell and the axon terminals target one of the four lobula plate layers. Both the dendrites and the axon terminals are limited to only one layer of their respective neuropil. We found two postmitotic transcription factors expressed in the young T4 and T5 cells, SoxN and Sox102F, which regulate the common features of all subtypes. These transcription factors are crucial for the proper morphology of the T4 and T5 cells, as well as the function of the adult neurons.