Detection of expansion motion can elicit different behaviors inDrosophila. During flight the flies can respond with avoidance turns or a landing response, while walking flies react with an escape jump. The flight avoidance turns as well as landing responses were suggested to depend on Hassenstein- Reichardt type motion detectors (Borst and Bahde, 1986; Reiser and Dickinson, 2013). This indicates, that T4 and T5 cells are important for avoidance flight turns and landing behavior.
We characterized the avoidance turns of fixed flyingDrosophilausing different looming stimuli. The flies avoided dark and bright approaching objects at a lateral position, over a wide range of velocities. The avoidance behavior was not dependent on the overall luminance change, but on opposing motion in at least two directions. We found the output of T4 and T5 cells to be
essential for the avoidance turns of flyingDrosophila. Moreover, flies with blocked T4 and T5 cells were unable to perform a landing response, elicited by a frontal looming stimulus. Therefore, we suspected that descending neurons involved in avoidance turns and landing behavior receive direct or indirect input from T4/T5.
Figure 3.5: Looming Sensitive Neurons
aCalcium imaging of LPLC2 neurons reacting to looming but not to a moving bar or wide-field
motion. Image modified from Klapoetke et al. (2017). bThe dendritic arms of a LPLC2 neuron in
the four lobula plate layers are oriented in four directions. cLC4 and LPLC2 are the main inputs to
the giant fiber with LC4 encoding angular velocity and LPLC2 encoding angular size of a looming
stimulus. Image modified from Ache et al. (2019). d Calcium imaging of LC16, LC6 and LC11
with a dark and a bright looming stimulus, LC6 and LC16 react strongly to dark looming. Image modified from Wu et al. (2016).
Looming sensitive neurons postsynaptic to T4/T5 cells were found in the Drosophila lobula
plate, namely the lobula plate/lobula columnar, type II or LPLC2 cells. Optogenetic activation of LPLC2 cells induced escape jumps or backward walking (Wu et al., 2016). The LPLC2 neurons respond specifically to looming stimuli, but not to whole-field motion or moving objects (Fig. 3.5 a) (Klapoetke et al., 2017). These neurons react strongly to outward motion in at least two of the cardinal directions, i.e. upwards and downwards motion, but are inhibited by inward motion. The inhibition is provided by Lpi neurons (Klapoetke et al., 2017). The LPLC2 neurons collect input from the four lobula plate layers and the lobula layers Lo3 to Lo5. The dendrites in the lobula plate have a striking morphology: four dendritic arms reach into every lobula plate layer, with the dendritic arms pointing in four different directions (Fig. 3.5 b) (Klapoetke et al., 2017). Their axons project into the central brain, where LPLC2 neurons synapse on the giant fiber descending neuron (Fig. 3.5 c) (Klapoetke et al., 2017; Ache et al., 2019). The giant fiber
is important to elicit short-duration, undirected escape jumps (von Reyn et al., 2014). Silencing LPLC2 neurons impairs such fast escape jumps (von Reyn et al., 2017; Ache et al., 2019). The giant fiber receives information from two main input cell types, LPLC2 and LC4. The LPLC2 neurons provide excitatory information about the angular size of a looming stimulus to the giant fiber and LC4 provides information about the angular velocity (Ache et al., 2019).
Descending neurons important for avoidance turns and landing responses could receive their input from LPLC2, since no other neurons postsynaptic to T4/T5 and sensitive to looming stimuli are known so far. There is no knowledge about additional neurons postsynaptic to LPLC2 besides the giant fiber, which could mediate avoidance turns or landing responses. Schnell et al. (2017) described a descending neuron responsive to looming stimuli and important for fast, saccade like turns during flight. This neuron could be important for collision avoidance turns, but the input neurons providing looming sensitive information are not known yet. Descending neurons impor- tant for avoidance turns, landing behavior or slow escape jumps might receive information about expansion motion from both, T4/T5 dependent and independent neurons.
3.3.1 Looming Sensitive Cells in the Lobula
Optogenetic activation of different lobula columnar cells induced avoidance behavior: activation of LC6, LC15, and LC16 resulted in escape jumps or backward walking of the flies (Wu et al., 2016). Similar to the giant fiber input LPLC2, the lobula columnar cells LC6 and LC16 are looming sensitive (Fig. 3.5 d) (Wu et al., 2016). LC6 and LC16 dendrites overlap in the lobula layers 4 to 6, and their axon terminals project to the same region in the central brain (Wu et al., 2016; Panser et al., 2016). In contrast to the giant fiber and its input neurons, blocking LC6 neurons reduced the proportion of long-duration escape jumps after looming stimulation (Williamson et al., 2018). This suggests the LC6 plays a role in the detection of slow expansion motion. However, a descending neuron mediating short-duration, targeted escape jumps is not found yet. While LPLC2 receives input from the lobula plate and the lobula, the dendrites of the different lobula columnar cells are restricted to the lobula. LC4 and LC6 both detect looming stimuli (Wu et al., 2016; von Reyn et al., 2017), likely without a T4/T5 dependent input.
Next to LPLC2, there is another neuron that receives input from T4 and T5 cells, the lobula plate/lobula columnar, type I or LPLC1. Since optogenetic activation of these cells strongly induced jumps, they are likely involved in avoidance behavior. The location of their axon terminals suggest, that they could connect to the giant fiber (Panser et al., 2016).
Reconstruction of electron microscopy data (Zheng et al., 2018) will reveal the connectivity between lobula neurons and descending neurons in the central brain. In addition, calcium imaging of the different lobula columnar neurons and also LPLC1 will clarify which neurons detect expansion motion. Blocking such neurons or activating them with optogenetic tools while measuring flight behavior could help to identify neurons involved in avoidance turns and landing behavior. More
driver lines for these neurons are available. With functional and anatomical data about lobula neurons and descending neurons in the central brain, the neuronal circuits underlying the different looming evoked behaviors will be solved.
3.3.2 Comparison to Looming Sensitive Neurons in other Arthropod Species
While it seems important for most animals to detect approaching objects, the induced behavior can differ substantially. An escape jump to avoid predators is only reasonable for an animal that is able to fly, while others might prefer not to move at all and rely on mimicry. Therefore, very different looming detecting neurons and subsequent descending neurons might have evolved for different arthropod species. While flies and locusts jump into the air, crabs escape walking and constantly adapt their direction and velocity during their escape (Oliva and Tomsic, 2012). While the looming detecting neurons of different arthropods differ in their anatomy and computations, there are some similarities: looming sensitive descending neurons receive input about angular velocity and angular size of the looming stimulus, resulting in a peak firing at the time before collision. Such a computation is performed by the lobula neuron LGMD of the locust, a lobula
neuron in the crab Neohelice, and the giant fiber of Drosophila (Gabbiani et al., 1999; von Reyn
et al., 2017; Oliva and Tomsic, 2014).
The input neurons of the locust LGMD neuron are supposed to detect information about local luminance change, not local motion (Jones and Gabbiani, 2010). A similar input is proposed for
looming sensitive lobula neurons of the crab Neohelice (Oliva and Tomsic, 2014). In contrast,
we found two different Drosophila behaviors elicited by looming stimuli to depend on the local
motion sensing T4 and T5 cells. In addition, the looming sensitive LPLC2 cells postsynaptic to T4 and T5 cells were demonstrated to be a main input to the giant fiber (Ache et al., 2019). Other looming sensitive neurons in the lobula ofDrosophila, like LC6 cells, likely detect looming stimuli through a different mechanism. Since the giant fiber receives input from lobula columnar cells and from the T4/T5 dependent LPLC2 neurons, one cell type providing angular velocity related input the other angular size related, different looming computations might work in parallel to ensure an optimal avoidance reaction. A large cell spanning over the lobula like the LGMD does not exist in Drosophila. Nevertheless, looming detection based on different inputs, either sensing local motion or local luminance changes, might be conserved across arthropod species.