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Complex tasks like hunting moving prey in an unpredictable environment require high levels of motor and sensory integration. An animal needs to detect and track suitable prey objects, measure their distance and orientation relative to its own position, and finally produce the correct motor output to approach and capture the prey. In the insect brain, the central complex (CX) is one target area where integration is likely to take place. In this study, we performed extracellular multi-unit recordings on the CX of freely hunting praying mantises (Tenodera sinensis). Initially, we recorded the neural activity of freely moving mantises as they hunted live prey. The recordings showed activity in cells that either reflected the mantis's own movements or the actions of a prey individual, which the mantises focused on. In the latter case, the activity increased as the prey moved and decreased when it stopped. Interestingly, cells ignored the movement of the other prey than the one to which the mantis attended. To obtain quantitative data, we generated simulated prey targets presented on an LCD screen positioned below the clear floor of the arena. The simulated target oscillated back and forth at various angles and distances. We identified populations of cells whose activity patterns were strongly linked to the appearance, movement, and relative position of the virtual prey. We refer to these as sensory responses. We also found cells whose activity preceded orientation movement toward the prey. We call these motor responses. Some cells showed both sensory and motor properties. Stimulation through tetrodes in some of the preparations could also generate similar movements. These results suggest the crucial importance of the CX to prey-capture behavior in predatory insects like the praying mantis and, hence, further emphasize its role in behaviorally and ecologically relevant contexts.
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Internal state effects on behavioral shifts in freely behaving praying mantises (Tenodera sinensis)
How we interact with our environment largely depends on both the external cues presented by our surroundings and the internal state from within. Internal states are the ever-changing physiological conditions that communicate the immediate survival needs and motivate the animal to behaviorally fulfill them. Satiety level constitutes such a state, and therefore has a dynamic influence on the output behaviors of an animal. In predatory insects like the praying mantis, hunting tactics, grooming, and mating have been shown to change hierarchical organization of behaviors depending on satiety. Here, we analyze behavior sequences of freely hunting praying mantises ( Tenodera sinensis ) to explore potential differences in sequential patterning of behavior as a correlate of satiety. First, our data supports previous work that showed starved praying mantises were not just more often attentive to prey, but also more often attentive to further prey. This was indicated by the increased time fraction spent in attentive bouts such as prey monitoring, head turns (to track prey), translations (closing the distance to the prey), and more strike attempts. With increasing satiety, praying mantises showed reduced time in these behaviors and exhibited them primarily towards close-proximity prey. Furthermore, our data demonstrates that during states of starvation, the praying mantis exhibits a stereotyped pattern of behavior that is highly motivated by prey capture. As satiety increased, the sequenced behaviors became more variable, indicating a shift away from the necessity of prey capture to more fluid presentations of behavior assembly.
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- Award ID(s):
- 1704436
- PAR ID:
- 10358694
- Editor(s):
- Louis, Matthieu
- Date Published:
- Journal Name:
- PLOS Computational Biology
- Volume:
- 17
- Issue:
- 12
- ISSN:
- 1553-7358
- Page Range / eLocation ID:
- e1009618
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1371/journal.pcbi.1009618
