Selectivity and plasticity in a sound-evoked male-male interaction in Drosophila.

During courtship, many animals, including insects, birds, fish, and mammals, utilize acoustic signals to transmit information about species identity. Although auditory communication is crucial across phyla, the neuronal and physiologic processes are poorly understood. Sound-evoked chaining behavior,...

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Main Authors: Jeonghyeon Yoon, Eriko Matsuo, Daichi Yamada, Hiroshi Mizuno, Takako Morimoto, Hiroyoshi Miyakawa, Setsuo Kinoshita, Hiroshi Ishimoto, Azusa Kamikouchi
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2013-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC3782482?pdf=render
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author Jeonghyeon Yoon
Eriko Matsuo
Daichi Yamada
Hiroshi Mizuno
Takako Morimoto
Hiroyoshi Miyakawa
Setsuo Kinoshita
Hiroshi Ishimoto
Azusa Kamikouchi
author_facet Jeonghyeon Yoon
Eriko Matsuo
Daichi Yamada
Hiroshi Mizuno
Takako Morimoto
Hiroyoshi Miyakawa
Setsuo Kinoshita
Hiroshi Ishimoto
Azusa Kamikouchi
author_sort Jeonghyeon Yoon
collection DOAJ
description During courtship, many animals, including insects, birds, fish, and mammals, utilize acoustic signals to transmit information about species identity. Although auditory communication is crucial across phyla, the neuronal and physiologic processes are poorly understood. Sound-evoked chaining behavior, a display of homosexual courtship behavior in Drosophila males, has long been used as an excellent model for analyzing auditory behavior responses, outcomes of acoustic perception and higher-order brain functions. Here we developed a new method, termed ChaIN (Chain Index Numerator), in which we use a computer-based auto detection system for chaining behavior. The ChaIN system can systematically detect the chaining behavior induced by a series of modified courtship song playbacks. Two evolutionarily related Drosophila species, Drosophila melanogaster and Drosophila simulans, exhibited dramatic selective increases in chaining behavior when exposed to specific auditory cues, suggesting that auditory discrimination processes are involved in the acceleration of chaining behavior. Prolonged monotonous pulse sounds containing courtship song components also induced high intense chaining behavior. Interestingly, the chaining behavior was gradually suppressed over time when song playback continued. This behavioral change is likely to be a plastic behavior and not a simple sensory adaptation or fatigue, because the suppression was released by applying a different pulse pattern. This behavioral plasticity is not a form of habituation because different modality stimuli did not recover the behavioral suppression. Intriguingly, this plastic behavior partially depended on the cAMP signaling pathway controlled by the rutabaga adenylyl cyclase gene that is important for learning and memory. Taken together, this study demonstrates the selectivity and behavioral kinetics of the sound-induced interacting behavior of Drosophila males, and provides a basis for the systematic analysis of genes and neural circuits underlying complex acoustic behavior.
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spelling doaj.art-e318d33deda3430a867c4e5f965d6fdf2022-12-21T18:47:37ZengPublic Library of Science (PLoS)PLoS ONE1932-62032013-01-0189e7428910.1371/journal.pone.0074289Selectivity and plasticity in a sound-evoked male-male interaction in Drosophila.Jeonghyeon YoonEriko MatsuoDaichi YamadaHiroshi MizunoTakako MorimotoHiroyoshi MiyakawaSetsuo KinoshitaHiroshi IshimotoAzusa KamikouchiDuring courtship, many animals, including insects, birds, fish, and mammals, utilize acoustic signals to transmit information about species identity. Although auditory communication is crucial across phyla, the neuronal and physiologic processes are poorly understood. Sound-evoked chaining behavior, a display of homosexual courtship behavior in Drosophila males, has long been used as an excellent model for analyzing auditory behavior responses, outcomes of acoustic perception and higher-order brain functions. Here we developed a new method, termed ChaIN (Chain Index Numerator), in which we use a computer-based auto detection system for chaining behavior. The ChaIN system can systematically detect the chaining behavior induced by a series of modified courtship song playbacks. Two evolutionarily related Drosophila species, Drosophila melanogaster and Drosophila simulans, exhibited dramatic selective increases in chaining behavior when exposed to specific auditory cues, suggesting that auditory discrimination processes are involved in the acceleration of chaining behavior. Prolonged monotonous pulse sounds containing courtship song components also induced high intense chaining behavior. Interestingly, the chaining behavior was gradually suppressed over time when song playback continued. This behavioral change is likely to be a plastic behavior and not a simple sensory adaptation or fatigue, because the suppression was released by applying a different pulse pattern. This behavioral plasticity is not a form of habituation because different modality stimuli did not recover the behavioral suppression. Intriguingly, this plastic behavior partially depended on the cAMP signaling pathway controlled by the rutabaga adenylyl cyclase gene that is important for learning and memory. Taken together, this study demonstrates the selectivity and behavioral kinetics of the sound-induced interacting behavior of Drosophila males, and provides a basis for the systematic analysis of genes and neural circuits underlying complex acoustic behavior.http://europepmc.org/articles/PMC3782482?pdf=render
spellingShingle Jeonghyeon Yoon
Eriko Matsuo
Daichi Yamada
Hiroshi Mizuno
Takako Morimoto
Hiroyoshi Miyakawa
Setsuo Kinoshita
Hiroshi Ishimoto
Azusa Kamikouchi
Selectivity and plasticity in a sound-evoked male-male interaction in Drosophila.
PLoS ONE
title Selectivity and plasticity in a sound-evoked male-male interaction in Drosophila.
title_full Selectivity and plasticity in a sound-evoked male-male interaction in Drosophila.
title_fullStr Selectivity and plasticity in a sound-evoked male-male interaction in Drosophila.
title_full_unstemmed Selectivity and plasticity in a sound-evoked male-male interaction in Drosophila.
title_short Selectivity and plasticity in a sound-evoked male-male interaction in Drosophila.
title_sort selectivity and plasticity in a sound evoked male male interaction in drosophila
url http://europepmc.org/articles/PMC3782482?pdf=render
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