Moonwalker Descending Neurons Mediate Visually Evoked Retreat in Drosophila

Abstract

Insects, like most animals, tend to steer away from imminent threats [1-7]. Drosophila melanogaster, for example, generally initiate an escape take-off in response to a looming visual stimulus, mimicking a potential predator [8]. The escape response to a visual threat is, however, flexible [9-12] and can alternatively consist of walking backward away from the perceived threat [11], which may be a more effective response to ambush predators such as nymphal praying mantids [7]. Flexibility in escape behavior may also add an element of unpredictability that makes it difficult for predators to anticipate or learn the prey's likely response [3-6]. Whereas the fly's escape jump has been well studied [8, 9, 13-18], the neuronal underpinnings of evasive walking remain largely unexplored. We previously reported the identification of a cluster of descending neurons-the moonwalker descending neurons (MDNs)-the activity of which is necessary and sufficient to trigger backward walking [19], as well as a population of visual projection neurons-the lobula columnar 16 (LC16) cells-that respond to looming visual stimuli and elicit backward walking and turning [11]. Given the similarity of their activation phenotypes, we hypothesized that LC16 neurons induce backward walking via MDNs and that turning while walking backward might reflect asymmetric activation of the left and right MDNs. Here, we present data from functional imaging, behavioral epistasis, and unilateral activation experiments that support these hypotheses. We conclude that LC16 and MDNs are critical components of the neural circuit that transduces threatening visual stimuli into directional locomotor output.

Visual recognition of the female body axis drives spatial elements of male courtship in Drosophila melanogaster

“…For instance, as a male approaches a stationary female during courtship, she would appear to be looming. LC4 and LC16 have previously been shown to respond to looming stimuli to generate escape responses [23,10,11]; here, we show that in the context of mating, males can also utilize these cell populations to drive distinct courtship behaviors. In contrast to previous studies that have focused on the role of female-generated movement in mediating male chase behaviors [6,7,8,9,12], our experiments indicate that visual cues play a much broader role in regulating spatial and temporal aspects of mating-related social interactions.…”

“…Recent studies have implicated several classes of Lobula Columnar (LC) visual projection neurons in the regulation of various visually-induced behaviors in the fly [10,11], including motion detection during specific aspects of courtship [12]. Consequently, we investigated whether LC neurons are also important for the regulation of different spatial and/or temporal aspects of the courtship ritual.…”

“…The activation or inhibition of LC neurons can elicit or prevent specific movements in flies, respectively [10,11]. To determine the types of movements required for proper male positioning during courtship, we therefore looked at average movement speeds when males were located at different angular positions around the female ( Figure 5A).…”

“…In diverse insect species, motion cues have been shown to be particularly important for triggering male chase behaviors during courtship [5,6,7,8,9]. These motion cues are detected and processed by visual projection neurons in the brain, which connect to downstream motor centers to generate relevant behavioral outputs [10,11,12]. While motion detection is important for keeping the male in proximity to a moving target during courtship, how specific visual cues and neural pathways might regulate the proper spatio-temporal coordination of other mating displays remains largely unknown.…”

Two brain pathways initiate distinct forward walking programs inDrosophila

“…Unilateral BPN activation induced straight forward walking, in contrast to turning phenotypes elicited by unilateral activation of other walking initiation neurons (P9, MDN and cricket DNs) (Böhm and Schildberger, 1992;Sen et al, 2017;Zorović and Hedwig, 2013). The BPN phenotype suggests that a neural pathway operating via unidentified DNs elicits straight forward walking.…”