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. 2023 May 9:14:1153913.
doi: 10.3389/fphys.2023.1153913. eCollection 2023.

Persistence of auditory modulation of wind-induced escape behavior in crickets

Affiliations

Persistence of auditory modulation of wind-induced escape behavior in crickets

Anhua Lu et al. Front Physiol. .

Abstract

Animals, including insects, change their innate escape behavior triggered by a specific threat stimulus depending on the environmental context to survive adaptively the predators' attack. This indicates that additional inputs from sensory organs of different modalities indicating surrounding conditions could affect the neuronal circuit responsible for the escape behavior. Field crickets, Gryllus bimaculatus, exhibit an oriented running or jumping escape in response to short air puff detected by the abdominal mechanosensory organ called cerci. Crickets also receive a high-frequency acoustic stimulus by their tympanal organs on their frontal legs, which suggests approaching bats as a predator. We have reported that the crickets modulate their wind-elicited escape running in the moving direction when they are exposed to an acoustic stimulus preceded by the air puff. However, it remains unclear how long the effects of auditory inputs indicating surrounding contexts last after the sound is terminated. In this study, we applied a short pulse (200 ms) of 15-kHz pure tone to the crickets in various intervals before the air-puff stimulus. The sound given 200 or 1000 ms before the air puff biased the wind-elicited escape running backward, like the previous studies using the longer and overlapped sound. But the sounds that started 2000 ms before and simultaneously with the air puff had little effect. In addition, the jumping probability was higher only when the delay of air puff to the sound was 1000 ms. These results suggest that the cricket could retain the auditory memory for at least one second and alter the motion choice and direction of the wind-elicited escape behavior.

Keywords: behavioral choice; contextual memory; cricket (Gryllus bimaculatus); crossmodal interactions; escape behavior; multisensory integration.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
Experimental apparatus and stimulation patterns for behavioral tests. (A) Servo-sphere treadmill system for stimulation and monitoring of the freely moving cricket. The air-puff stimulus was applied from the right or left side of the cricket, which was specified by controlling the orientation of the cricket’s body against the air nozzle with the servo-sphere treadmill system that was closed-loop controlled based on the high-speed camera image of the cricket. (B) Temporal arrangement of the air-puff and acoustic stimuli for the five different patterns. For the control pattern, only single air-puff stimuli were applied without the acoustic stimulus. For patterns 1-4, a 15-kHz pure tone sound of 200-ms duration was applied from a loudspeaker above the air nozzle, and the air-puff stimulus was initiated 0, 200, 1000, and 2000 ms after the onset of the acoustic stimulus, respectively.
FIGURE 2
FIGURE 2
Auditory effects on the response probability and the action selection between running and jumping. (A, B) The probability of escape response in all trials (A) and the jumping probability in the responding trials (B) for the combined stimulation patterns (blue) and control (gray). Small dots connected by lines indicate the mean of the locomotion parameters for each individual. Black squares indicate the average of the data of all individuals. *p < 0.05, Wilcoxon rank-sum test. N = 15 individuals for each combined stimulation pattern.
FIGURE 3
FIGURE 3
Movements in the running escape responses. (A) Typical running trajectories of given individuals in the running response to air puffs combined with and without acoustic stimulus. Gray traces indicate the response in control. Blue traces indicate the response to air-puff combined with tone sound, 0 ms (pattern 1), 200 ms (pattern 2), 1000 ms (pattern 3), and 2000 ms (pattern 4) before the air-puff onset. The trajectories were combined data of the responses to left and right stimuli. The trajectories for the control condition were displayed against the air puff from the right side, and those for the combined stimulation conditions were displayed against the air puff from the left side. (B) Distributions of running direction for different stimulation patterns. Gray bars represent the data for controls, and blue bars represent those for patterns 1, 2, 3, and 4. N = 15 individuals for control and each acoustic stimulation pattern.
FIGURE 4
FIGURE 4
Auditory effects on the movement direction in the running response. (A) Movement direction for control (gray) and combined stimulation patterns (blue). Small dots connected by lines indicate the mean angle of the movement directions for each individual. Black squares indicate the average of the data of all individuals. The direction opposite to the air puff is indicated as positive. *p < 0.05, **p < 0.01, paired t-test. (B) Changes in movement direction by acoustic stimulation. Small gray dots represent the mean of the data of each individual. *p < 0.05, **p < 0.01 unpaired t-test with Bonferroni correction. N = 15 individuals for each acoustic stimulation pattern.
FIGURE 5
FIGURE 5
No effects of acoustic stimulation on other locomotion parameters for the running response. (A–C) Maximum movement velocity (A), movement distance (B), and reaction time (C) in the escape running responses for the different patterns of combined stimulation (blue) and control (gray). Small dots connected by lines indicate the mean of the locomotion parameters for each individual. Black squares indicate the average of the data of all individuals. There was no significant difference in these parameters between combined stimulation patterns (1–4) and control (paired t-test). N = 15 individuals for control and each acoustic stimulation pattern.
FIGURE 6
FIGURE 6
No effects of acoustic stimulation on the locomotion in the jumping response. (A–D) Movement direction (A), maximum movement velocity (B), movement distance (C), and reaction time (D) in the escape jumping responses for the different patterns of combined stimulation (blue) and control (gray). Small dots connected by lines indicate the mean of the locomotion parameters for each individual. Black squares indicate the average of the data of all individuals. There was no significant difference in these parameters between combined stimulation patterns (1–4) and control (unpaired t-test). N = 11 and 11 (pattern 1), 8 and 11 (pattern 2), 12 and 12 (pattern 3), and 12 and 11 (pattern 4) individuals for control and each combined stimulation, respectively.

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Grants and funding

This work was supported by funding to HO from JSPS and MEXT KAKENHI grants 16H06544, 21K06259, and 21H05295.

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