Responses of cricket cercal interneurons to realistic naturalistic stimuli in the field

Dupuy, Fabienne; Steinmann, Thomas; Pierre, Dominique; Christidès, Jean-Philippe; Cummins, Graham I.; Lazzari, Cláudio R.; Miller, John P.; Casas, Jérôme

doi:10.1242/jeb.067405

Cited by 21 publications

(17 citation statements)

References 30 publications

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“…This contrasts strongly with the situation for similar studies on mouth movements in suction feeding fishes during closerange prey capture [33]. For prey crickets, our findings suggest that future studies should focus on the hitherto neglected aspects of danger identification and motor control during escape, echoing recent neurophysiological studies on the cercal response to stimuli with various spatial and temporal patterns [34,35]. These aspects have been little studied in most invertebrate predator-prey systems.…”

Section: Discussioncontrasting

confidence: 93%

Predator-induced flow disturbances alert prey, from the onset of an attack

Casas

Steinmann

2014

Proc. R. Soc. B.

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Many prey species, from soil arthropods to fish, perceive the approach of predators, allowing them to escape just in time. Thus, prey capture is as important to predators as prey finding. We extend an existing framework for understanding the conjoint trajectories of predator and prey after encounters, by estimating the ratio of predator attack and prey danger perception distances, and apply it to wolf spiders attacking wood crickets. Disturbances to air flow upstream from running spiders, which are sensed by crickets, were assessed by computational fluid dynamics with the finite-elements method for a much simplified spider model: body size, speed and ground effect were all required to obtain a faithful representation of the aerodynamic signature of the spider, with the legs making only a minor contribution. The relationship between attack speed and the maximal distance at which the cricket can perceive the danger is parabolic; it splits the space defined by these two variables into regions differing in their values for this ratio. For this biological interaction, the ratio is no greater than one, implying immediate perception of the danger, from the onset of attack. Particular attention should be paid to the ecomechanical aspects of interactions with such small ratio, because of the high degree of bidirectional coupling of the behaviour of the two protagonists. This conclusion applies to several other predator-prey systems with sensory ecologies based on flow sensing, in air and water.

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Section: Discussioncontrasting

confidence: 93%

Predator-induced flow disturbances alert prey, from the onset of an attack

Casas

Steinmann

2014

Proc. R. Soc. B.

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“…Although some sensory hairs and hair-like organs that mediate anemotaxis in multiple species have been identified [8][9][10][11], the neural underpinnings of how information about the wind direction is transformed into directional behavioral responses during anemotaxis in the CNS have been understudied.…”

Section: Introductionmentioning

confidence: 99%

Neural Substrates of Drosophila Larval Anemotaxis

et al. 2019

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Graphical AbstractHighlights d Drosophila larvae perform negative anemotaxis d To anemotax, larvae modulate the turn rate, size, and direction as in other taxis d Chordotonal and multidendritic class III sensory neurons together mediate anemotaxis d The anemotactic circuitry involves both the nerve cord and the brain SUMMARY Animals use sensory information to move toward more favorable conditions. Drosophila larvae can move up or down gradients of odors (chemotax), light (phototax), and temperature (thermotax) by modulating the probability, direction, and size of turns based on sensory input. Whether larvae can anemotax in gradients of mechanosensory cues is unknown. Further, although many of the sensory neurons that mediate taxis have been described, the central circuits are not well understood. Here, we used highthroughput, quantitative behavioral assays to demonstrate Drosophila larvae anemotax in gradients of wind speeds and to characterize the behavioral strategies involved. We found that larvae modulate the probability, direction, and size of turns to move away from higher wind speeds. This suggests that similar central decision-making mechanisms underlie taxis in somatosensory and other sensory modalities. By silencing the activity of single or very few neuron types in a behavioral screen, we found two sensory (chordotonal and multidendritic class III) and six nerve cord neuron types involved in anemotaxis. We reconstructed the identified neurons in an electron microscopy volume that spans the entire larval nervous system and found they received direct input from the mechanosensory neurons or from each other. In this way, we identified local interneurons and firstand second-order subesophageal zone (SEZ) and brain projection neurons. Finally, silencing a dopaminergic brain neuron type impairs anemotaxis. These findings suggest that anemotaxis involves both nerve cord and brain circuits. The candidate neurons and circuitry identified in our study provide a basis for future detailed mechanistic understanding of the circuit principles of anemotaxis. CATMAID https://catmaid.readthedocs.org/ [32] MATLAB http://www.mathworks.com [45, 69] Current Biology 29, 554-566.e1-e4, February 18, 2019 e1

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“…We used a wide range of air current velocities (0.014 -0.56 m/s) and durations (20 -1,000 ms), which cover the velocities and durations given for singing crickets (Kämper 1984) and for disturbance effects by approaching predators (Dupuy et al 2012;Gnatzy and Heußlein 1986;Gnatzy and Kämper 1990;Triblehorn and Yager 2006). The stimuli used here were a uniform onset of bulk air movement toward the cerci, from the back to the front of the animal, which does not represent the natural situation.…”

Section: Discussionmentioning

confidence: 99%

Impact of cercal air currents on singing motor pattern generation in the cricket (Gryllus bimaculatusDeGeer)

Jacob

Hedwig

2015

Journal of Neurophysiology

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Jacob PF, Hedwig B. Impact of cercal air currents on singing motor pattern generation in the cricket (Gryllus bimaculatus DeGeer). J Neurophysiol 114: 2649 -2660, 2015. First published September 2, 2015; doi:10.1152/jn.00669.2015.-The cercal system of crickets detects low-frequency air currents produced by approaching predators and self-generated air currents during singing, which may provide sensory feedback to the singing motor network. We analyzed the effect of cercal stimulation on singing motor pattern generation to reveal the response of a singing interneuron to predator-like signals and to elucidate the possible role of self-generated air currents during singing. In fictive singing males, we recorded an interneuron of the singing network while applying air currents to the cerci; additionally, we analyzed the effect of abolishing the cercal system in freely singing males. In fictively singing crickets, the effect of short air stimuli is either to terminate prematurely or to lengthen the interchirp interval, depending on their phase in the chirp cycle. Within our stimulation paradigm, air stimuli of different velocities and durations always elicited an inhibitory postsynaptic potential in the singing interneuron. Current injection in the singing interneuron elicited singing motor activity, even during the air current-evoked inhibitory input from the cercal pathway. The disruptive effects of air stimuli on the fictive singing pattern and the inhibitory response of the singing interneuron point toward the cercal system being involved in initiating avoidance responses in singing crickets, according to the established role of cerci in a predator escape pathway. After abolishing the activity of the cercal system, the timing of natural singing activity was not significantly altered. Our study provides no evidence that selfgenerated cercal sensory activity has a feedback function for singing motor pattern generation. cercal sensory system; air stimulus; singing central pattern generator interneuron; escape response TERRESTRIAL ANIMALS are constantly subjected to air currents, which, among others, can be of atmospheric origin, produced by approaching predators and conspecifics, or self-generated.Crickets, cockroaches, and locusts detect air currents through the cerci, two appendages at the rear of the abdomen (Edwards and Palka 1974) that carry up to 2,000 mechanosensitive filiform hairs (Chiba et al. 1992). Each filiform hair is innervated by a single sensory neuron, which makes synaptic connections with ascending interneurons, like the giant interneurons (GIs), in the terminal abdominal ganglion (TAG; Edwards and Palka 1974). Stimulation of the cercal pathway with salient air currents as generated by predators triggers escape responses and aggressive and freezing reactions and alters the singing behavior in male crickets (Baba and Shimozawa 1997;Dambach et al. 1983;Kohstall-Schnell and Gras 1994;Lewkiewicz and Zuk 2004;Matsuura et al. 2002). Air currents directed to the cerci evoke silencing responses in singing ...

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Responses of cricket cercal interneurons to realistic naturalistic stimuli in the field

Cited by 21 publications

References 30 publications

Predator-induced flow disturbances alert prey, from the onset of an attack

Predator-induced flow disturbances alert prey, from the onset of an attack

Neural Substrates of Drosophila Larval Anemotaxis

Impact of cercal air currents on singing motor pattern generation in the cricket (Gryllus bimaculatusDeGeer)

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