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Parallel Processing of Olfactory and Mechanosensory Information in the Honey Bee Antennal Lobe

In insects, neuronal responses to clean air have so far been reported only episodically in moths. Here we present results obtained by fast two-photon calcium imaging in the honey bee Apis mellifera, indicating a substantial involvement of the antennal lobe, the first olfactory neuropil, in the proce...

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Autores principales: Tiraboschi, Ettore, Leonardelli, Luana, Segata, Gianluca, Haase, Albrecht
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8691435/
https://www.ncbi.nlm.nih.gov/pubmed/34950059
http://dx.doi.org/10.3389/fphys.2021.790453
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author Tiraboschi, Ettore
Leonardelli, Luana
Segata, Gianluca
Haase, Albrecht
author_facet Tiraboschi, Ettore
Leonardelli, Luana
Segata, Gianluca
Haase, Albrecht
author_sort Tiraboschi, Ettore
collection PubMed
description In insects, neuronal responses to clean air have so far been reported only episodically in moths. Here we present results obtained by fast two-photon calcium imaging in the honey bee Apis mellifera, indicating a substantial involvement of the antennal lobe, the first olfactory neuropil, in the processing of mechanical stimuli. Clean air pulses generate a complex pattern of glomerular activation that provides a code for stimulus intensity and dynamics with a similar level of stereotypy as observed for the olfactory code. Overlapping the air pulses with odor stimuli reveals a superposition of mechanosensory and odor response codes with high contrast. On the mechanosensitive signal, modulations were observed in the same frequency regime as the oscillatory motion of the antennae, suggesting a possible way to detect odorless airflow directions. The transduction of mechanosensory information via the insect antennae has so far been attributed primarily to Johnston’s organ in the pedicel of the antenna. The possibility that the antennal lobe activation by clean air originates from Johnston’s organ could be ruled out, as the signal is suppressed by covering the surfaces of the otherwise freely moving and bending antennae, which should leave Johnston’s organ unaffected. The tuning curves of individual glomeruli indicate increased sensitivity at low-frequency mechanical oscillations as produced by the abdominal motion in waggle dance communication, suggesting a further potential function of this mechanosensory code. The discovery that the olfactory system can sense both odors and mechanical stimuli has recently been made also in mammals. The results presented here give hope that studies on insects can make a fundamental contribution to the cross-taxa understanding of this dual function, as only a few thousand neurons are involved in their brains, all of which are accessible by in vivo optical imaging.
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spelling pubmed-86914352021-12-22 Parallel Processing of Olfactory and Mechanosensory Information in the Honey Bee Antennal Lobe Tiraboschi, Ettore Leonardelli, Luana Segata, Gianluca Haase, Albrecht Front Physiol Physiology In insects, neuronal responses to clean air have so far been reported only episodically in moths. Here we present results obtained by fast two-photon calcium imaging in the honey bee Apis mellifera, indicating a substantial involvement of the antennal lobe, the first olfactory neuropil, in the processing of mechanical stimuli. Clean air pulses generate a complex pattern of glomerular activation that provides a code for stimulus intensity and dynamics with a similar level of stereotypy as observed for the olfactory code. Overlapping the air pulses with odor stimuli reveals a superposition of mechanosensory and odor response codes with high contrast. On the mechanosensitive signal, modulations were observed in the same frequency regime as the oscillatory motion of the antennae, suggesting a possible way to detect odorless airflow directions. The transduction of mechanosensory information via the insect antennae has so far been attributed primarily to Johnston’s organ in the pedicel of the antenna. The possibility that the antennal lobe activation by clean air originates from Johnston’s organ could be ruled out, as the signal is suppressed by covering the surfaces of the otherwise freely moving and bending antennae, which should leave Johnston’s organ unaffected. The tuning curves of individual glomeruli indicate increased sensitivity at low-frequency mechanical oscillations as produced by the abdominal motion in waggle dance communication, suggesting a further potential function of this mechanosensory code. The discovery that the olfactory system can sense both odors and mechanical stimuli has recently been made also in mammals. The results presented here give hope that studies on insects can make a fundamental contribution to the cross-taxa understanding of this dual function, as only a few thousand neurons are involved in their brains, all of which are accessible by in vivo optical imaging. Frontiers Media S.A. 2021-12-07 /pmc/articles/PMC8691435/ /pubmed/34950059 http://dx.doi.org/10.3389/fphys.2021.790453 Text en Copyright © 2021 Tiraboschi, Leonardelli, Segata and Haase. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Physiology
Tiraboschi, Ettore
Leonardelli, Luana
Segata, Gianluca
Haase, Albrecht
Parallel Processing of Olfactory and Mechanosensory Information in the Honey Bee Antennal Lobe
title Parallel Processing of Olfactory and Mechanosensory Information in the Honey Bee Antennal Lobe
title_full Parallel Processing of Olfactory and Mechanosensory Information in the Honey Bee Antennal Lobe
title_fullStr Parallel Processing of Olfactory and Mechanosensory Information in the Honey Bee Antennal Lobe
title_full_unstemmed Parallel Processing of Olfactory and Mechanosensory Information in the Honey Bee Antennal Lobe
title_short Parallel Processing of Olfactory and Mechanosensory Information in the Honey Bee Antennal Lobe
title_sort parallel processing of olfactory and mechanosensory information in the honey bee antennal lobe
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8691435/
https://www.ncbi.nlm.nih.gov/pubmed/34950059
http://dx.doi.org/10.3389/fphys.2021.790453
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