Anatomic and Physiologic Heterogeneity of Subgroup-A Auditory Sensory Neurons in Fruit Flies

The antennal ear of the fruit fly detects acoustic signals in intraspecific communication, such as the courtship song and agonistic sounds. Among the five subgroups of mechanosensory neurons in the fly ear, subgroup-A neurons respond maximally to vibrations over a wide frequency range between 100 an...

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Main Authors: Yuki Ishikawa, Natsuki Okamoto, Mizuki Nakamura, Hyunsoo Kim, Azusa Kamikouchi
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-06-01
Series:Frontiers in Neural Circuits
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fncir.2017.00046/full
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spelling doaj-74d64d6725814d89a71529e9ef44f6d12020-11-25T00:22:28ZengFrontiers Media S.A.Frontiers in Neural Circuits1662-51102017-06-011110.3389/fncir.2017.00046274969Anatomic and Physiologic Heterogeneity of Subgroup-A Auditory Sensory Neurons in Fruit FliesYuki IshikawaNatsuki OkamotoMizuki NakamuraHyunsoo KimAzusa KamikouchiThe antennal ear of the fruit fly detects acoustic signals in intraspecific communication, such as the courtship song and agonistic sounds. Among the five subgroups of mechanosensory neurons in the fly ear, subgroup-A neurons respond maximally to vibrations over a wide frequency range between 100 and 1,200 Hz. The functional organization of the neural circuit comprised of subgroup-A neurons, however, remains largely unknown. In the present study, we used 11 GAL4 strains that selectively label subgroup-A neurons and explored the diversity of subgroup-A neurons by combining single-cell anatomic analysis and Ca2+ imaging. Our findings indicate that the subgroup-A neurons that project into various combinations of subareas in the brain are more anatomically diverse than previously described. Subgroup-A neurons were also physiologically diverse, and some types were tuned to a narrow frequency range, suggesting that the response of subgroup-A neurons to sounds of a wide frequency range is due to the existence of several types of subgroup-A neurons. Further, we found that an auditory behavioral response to the courtship song of flies was attenuated when most subgroup-A neurons were silenced. Together, these findings characterize the heterogeneous functional organization of subgroup-A neurons, which might facilitate species-specific acoustic signal detection.http://journal.frontiersin.org/article/10.3389/fncir.2017.00046/fullJohnston's organDrosophilaCa2+ imagingmechanosensoryinsectauditory behavior
collection DOAJ
language English
format Article
sources DOAJ
author Yuki Ishikawa
Natsuki Okamoto
Mizuki Nakamura
Hyunsoo Kim
Azusa Kamikouchi
spellingShingle Yuki Ishikawa
Natsuki Okamoto
Mizuki Nakamura
Hyunsoo Kim
Azusa Kamikouchi
Anatomic and Physiologic Heterogeneity of Subgroup-A Auditory Sensory Neurons in Fruit Flies
Frontiers in Neural Circuits
Johnston's organ
Drosophila
Ca2+ imaging
mechanosensory
insect
auditory behavior
author_facet Yuki Ishikawa
Natsuki Okamoto
Mizuki Nakamura
Hyunsoo Kim
Azusa Kamikouchi
author_sort Yuki Ishikawa
title Anatomic and Physiologic Heterogeneity of Subgroup-A Auditory Sensory Neurons in Fruit Flies
title_short Anatomic and Physiologic Heterogeneity of Subgroup-A Auditory Sensory Neurons in Fruit Flies
title_full Anatomic and Physiologic Heterogeneity of Subgroup-A Auditory Sensory Neurons in Fruit Flies
title_fullStr Anatomic and Physiologic Heterogeneity of Subgroup-A Auditory Sensory Neurons in Fruit Flies
title_full_unstemmed Anatomic and Physiologic Heterogeneity of Subgroup-A Auditory Sensory Neurons in Fruit Flies
title_sort anatomic and physiologic heterogeneity of subgroup-a auditory sensory neurons in fruit flies
publisher Frontiers Media S.A.
series Frontiers in Neural Circuits
issn 1662-5110
publishDate 2017-06-01
description The antennal ear of the fruit fly detects acoustic signals in intraspecific communication, such as the courtship song and agonistic sounds. Among the five subgroups of mechanosensory neurons in the fly ear, subgroup-A neurons respond maximally to vibrations over a wide frequency range between 100 and 1,200 Hz. The functional organization of the neural circuit comprised of subgroup-A neurons, however, remains largely unknown. In the present study, we used 11 GAL4 strains that selectively label subgroup-A neurons and explored the diversity of subgroup-A neurons by combining single-cell anatomic analysis and Ca2+ imaging. Our findings indicate that the subgroup-A neurons that project into various combinations of subareas in the brain are more anatomically diverse than previously described. Subgroup-A neurons were also physiologically diverse, and some types were tuned to a narrow frequency range, suggesting that the response of subgroup-A neurons to sounds of a wide frequency range is due to the existence of several types of subgroup-A neurons. Further, we found that an auditory behavioral response to the courtship song of flies was attenuated when most subgroup-A neurons were silenced. Together, these findings characterize the heterogeneous functional organization of subgroup-A neurons, which might facilitate species-specific acoustic signal detection.
topic Johnston's organ
Drosophila
Ca2+ imaging
mechanosensory
insect
auditory behavior
url http://journal.frontiersin.org/article/10.3389/fncir.2017.00046/full
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