Multisite imaging of neural activity using a genetically encoded calcium sensor in the honey bee
Understanding of the neural bases for complex behaviors in Hymenoptera insect species has been limited by a lack of tools that allow measuring neuronal activity simultaneously in different brain regions. Here, we developed the first pan-neuronal genetic driver in a Hymenopteran model organism, the h...
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description | Understanding of the neural bases for complex behaviors in Hymenoptera insect species has been limited by a lack of tools that allow measuring neuronal activity simultaneously in different brain regions. Here, we developed the first pan-neuronal genetic driver in a Hymenopteran model organism, the honey bee, and expressed the calcium indicator GCaMP6f under the control of the honey bee synapsin promoter. We show that GCaMP6f is widely expressed in the honey bee brain, allowing to record neural activity from multiple brain regions. To assess the power of this tool, we focused on the olfactory system, recording simultaneous responses from the antennal lobe, and from the more poorly investigated lateral horn (LH) and mushroom body (MB) calyces. Neural responses to 16 distinct odorants demonstrate that odorant quality (chemical structure) and quantity are faithfully encoded in the honey bee antennal lobe. In contrast, odor coding in the LH departs from this simple physico-chemical coding, supporting the role of this structure in coding the biological value of odorants. We further demonstrate robust neural responses to several bee pheromone odorants, key drivers of social behavior, in the LH. Combined, these brain recordings represent the first use of a neurogenetic tool for recording large-scale neural activity in a eusocial insect and will be of utility in assessing the neural underpinnings of olfactory and other sensory modalities and of social behaviors and cognitive abilities. |
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Here, we developed the first pan-neuronal genetic driver in a Hymenopteran model organism, the honey bee, and expressed the calcium indicator GCaMP6f under the control of the honey bee synapsin promoter. We show that GCaMP6f is widely expressed in the honey bee brain, allowing to record neural activity from multiple brain regions. To assess the power of this tool, we focused on the olfactory system, recording simultaneous responses from the antennal lobe, and from the more poorly investigated lateral horn (LH) and mushroom body (MB) calyces. Neural responses to 16 distinct odorants demonstrate that odorant quality (chemical structure) and quantity are faithfully encoded in the honey bee antennal lobe. In contrast, odor coding in the LH departs from this simple physico-chemical coding, supporting the role of this structure in coding the biological value of odorants. We further demonstrate robust neural responses to several bee pheromone odorants, key drivers of social behavior, in the LH. Combined, these brain recordings represent the first use of a neurogenetic tool for recording large-scale neural activity in a eusocial insect and will be of utility in assessing the neural underpinnings of olfactory and other sensory modalities and of social behaviors and cognitive abilities.</description><identifier>ISSN: 1545-7885</identifier><identifier>ISSN: 1544-9173</identifier><identifier>EISSN: 1545-7885</identifier><identifier>DOI: 10.1371/journal.pbio.3001984</identifier><identifier>PMID: 36719927</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animal cognition ; Animals ; Antennal lobe ; Apis mellifera ; Aroma compounds ; Bees ; Bees - genetics ; Behavior ; Biochemistry, Molecular Biology ; Biology and Life Sciences ; Biosensors ; Brain ; Brain - physiology ; Brain research ; Calcium ; Coding ; Cognitive ability ; Eusociality ; Gene expression ; Genetic aspects ; Genetic code ; Genetic engineering ; Genomes ; Genomics ; Honey ; Honeybee ; Insects ; Life Sciences ; Luteinizing hormone ; Methods and Resources ; Mushroom bodies ; Neural circuitry ; Neural coding ; Neurobiology ; Neuroimaging ; Neurons ; Neurons and Cognition ; Odorants ; Odors ; Olfactory system ; Pheromones - genetics ; Physical Sciences ; Physiological aspects ; Proteins ; Recording ; Research and Analysis Methods ; Sensors ; Sensory evaluation ; Smell - genetics ; Social behavior ; Social Sciences ; Synapsin</subject><ispartof>PLoS biology, 2023-01, Vol.21 (1), p.e3001984-e3001984</ispartof><rights>Copyright: © 2023 Carcaud et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</rights><rights>COPYRIGHT 2023 Public Library of Science</rights><rights>2023 Carcaud et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>2023 Carcaud et al 2023 Carcaud et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c729t-cec17450370516b000e560a8cd79204c663b8bdc5b92d0693acc1fe250c5e2de3</citedby><cites>FETCH-LOGICAL-c729t-cec17450370516b000e560a8cd79204c663b8bdc5b92d0693acc1fe250c5e2de3</cites><orcidid>0000-0003-3672-9963</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9917304/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9917304/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,724,777,781,861,882,2096,2915,23847,27905,27906,53772,53774,79349,79350</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36719927$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-04295196$$DView record in HAL$$Hfree_for_read</backlink></links><search><contributor>Chittka, Lars</contributor><creatorcontrib>Carcaud, Julie</creatorcontrib><creatorcontrib>Otte, Marianne</creatorcontrib><creatorcontrib>Grünewald, Bernd</creatorcontrib><creatorcontrib>Haase, Albrecht</creatorcontrib><creatorcontrib>Sandoz, Jean-Christophe</creatorcontrib><creatorcontrib>Beye, Martin</creatorcontrib><title>Multisite imaging of neural activity using a genetically encoded calcium sensor in the honey bee</title><title>PLoS biology</title><addtitle>PLoS Biol</addtitle><description>Understanding of the neural bases for complex behaviors in Hymenoptera insect species has been limited by a lack of tools that allow measuring neuronal activity simultaneously in different brain regions. 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genetics</topic><topic>Behavior</topic><topic>Biochemistry, Molecular Biology</topic><topic>Biology and Life Sciences</topic><topic>Biosensors</topic><topic>Brain</topic><topic>Brain - physiology</topic><topic>Brain research</topic><topic>Calcium</topic><topic>Coding</topic><topic>Cognitive ability</topic><topic>Eusociality</topic><topic>Gene expression</topic><topic>Genetic aspects</topic><topic>Genetic code</topic><topic>Genetic engineering</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Honey</topic><topic>Honeybee</topic><topic>Insects</topic><topic>Life Sciences</topic><topic>Luteinizing hormone</topic><topic>Methods and Resources</topic><topic>Mushroom bodies</topic><topic>Neural circuitry</topic><topic>Neural coding</topic><topic>Neurobiology</topic><topic>Neuroimaging</topic><topic>Neurons</topic><topic>Neurons and Cognition</topic><topic>Odorants</topic><topic>Odors</topic><topic>Olfactory system</topic><topic>Pheromones - genetics</topic><topic>Physical Sciences</topic><topic>Physiological aspects</topic><topic>Proteins</topic><topic>Recording</topic><topic>Research and Analysis Methods</topic><topic>Sensors</topic><topic>Sensory evaluation</topic><topic>Smell - 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Here, we developed the first pan-neuronal genetic driver in a Hymenopteran model organism, the honey bee, and expressed the calcium indicator GCaMP6f under the control of the honey bee synapsin promoter. We show that GCaMP6f is widely expressed in the honey bee brain, allowing to record neural activity from multiple brain regions. To assess the power of this tool, we focused on the olfactory system, recording simultaneous responses from the antennal lobe, and from the more poorly investigated lateral horn (LH) and mushroom body (MB) calyces. Neural responses to 16 distinct odorants demonstrate that odorant quality (chemical structure) and quantity are faithfully encoded in the honey bee antennal lobe. In contrast, odor coding in the LH departs from this simple physico-chemical coding, supporting the role of this structure in coding the biological value of odorants. We further demonstrate robust neural responses to several bee pheromone odorants, key drivers of social behavior, in the LH. Combined, these brain recordings represent the first use of a neurogenetic tool for recording large-scale neural activity in a eusocial insect and will be of utility in assessing the neural underpinnings of olfactory and other sensory modalities and of social behaviors and cognitive abilities.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>36719927</pmid><doi>10.1371/journal.pbio.3001984</doi><orcidid>https://orcid.org/0000-0003-3672-9963</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animal cognition Animals Antennal lobe Apis mellifera Aroma compounds Bees Bees - genetics Behavior Biochemistry, Molecular Biology Biology and Life Sciences Biosensors Brain Brain - physiology Brain research Calcium Coding Cognitive ability Eusociality Gene expression Genetic aspects Genetic code Genetic engineering Genomes Genomics Honey Honeybee Insects Life Sciences Luteinizing hormone Methods and Resources Mushroom bodies Neural circuitry Neural coding Neurobiology Neuroimaging Neurons Neurons and Cognition Odorants Odors Olfactory system Pheromones - genetics Physical Sciences Physiological aspects Proteins Recording Research and Analysis Methods Sensors Sensory evaluation Smell - genetics Social behavior Social Sciences Synapsin |
title | Multisite imaging of neural activity using a genetically encoded calcium sensor in the honey bee |
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