Immunohistochemical Approach to Understanding the Organization of the Olfactory System in the Cuttlefish, Sepia officinalis

Alexia T. Scaros; Roger P. Croll; Sébastien Baratte

doi:10.1021/acschemneuro.8b00021

Immunohistochemical Approach to Understanding the Organization of the Olfactory System in the Cuttlefish, Sepia officinalis

Alexia T. Scaros, Roger P. Croll, Sébastien Baratte

Medicine

Medicine

Résultat de recherche: Article › examen par les pairs

10 Citations (Scopus)

Résumé

Cephalopods are nontraditional but captivating models of invertebrate neurobiology, particularly in evolutionary comparisons. Cephalopod olfactory systems have striking similarities and fundamental differences with vertebrates, arthropods, and gastropods, raising questions about the ancestral origins of those systems. We describe here the organization and development of the olfactory system of the common cuttlefish, Sepia officinalis, using immunohistochemistry and in situ hybridization. FMRFamide and/or related peptides and histamine are putative neurotransmitters in olfactory sensory neurons. Other neurotransmitters, including serotonin and APGWamide within the olfactory and other brain lobes, suggest efferent control of olfactory input and/or roles in the processing of olfactory information. The distributions of neurotransmitters, along with staining patterns of phalloidin, anti-acetylated α-tubulin, and a synaptotagmin riboprobe, help to clarify the structure of the olfactory lobe. We discuss a key difference, the lack of identifiable olfactory glomeruli, in cuttlefish in comparison to other models, and suggest its implications for the evolution of olfaction.

Langue d'origine	English
Pages (de-à)	2074-2088
Nombre de pages	15
Journal	ACS Chemical Neuroscience
Volume	9
Numéro de publication	8
DOI	https://doi.org/10.1021/acschemneuro.8b00021
Statut de publication	Published - août 15 2018

Note bibliographique

Funding Information:
*E-mail: baratte@mnhn.fr. ORCID Roger P. Croll: 0000-0002-9846-0923 Author Contributions The manuscript has been read and approved by all named authors, and there are no other persons who satisfied the criteria for authorship but are not listed. We further confirm that the order of authors listed in the manuscript has been approved by all of us. All authors had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Acquisition of data: A.T.S., S.B., and R.P.C. Analysis and interpretation of data: A.T.S., S.B., and R.P.C. Drafting of the manuscript: A.T.S., S.B., and R.P.C. Critical revision of the manuscript for important intellectual content: A.T.S., R.P.C., and S.B. Funding Natural Sciences and Engineering Research Council of Canada, Laboratoire Biologie des Organismes et Ecosysteḿ es Aqua-tiques in Paris (Le Centre National de la Recherche Scientifique, UMR 7208, Museum National d’Histoire Nature-lle, Institut de Recherche pour le Developement France, 207, Université Pierre et Marie Curie), the France Canada Research Fund (2013), the Mitacs Globalink Research Program (2015), the province of Nova Scotia for the Graduate Scholarship (2017), and Dalhousie University for the International Differential Fee Scholarship (2017). Notes The authors declare no competing financial interest.

Publisher Copyright:
© 2018 American Chemical Society.

ASJC Scopus Subject Areas

Biochemistry
Physiology
Cognitive Neuroscience
Cell Biology

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10.1021/acschemneuro.8b00021

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title = "Immunohistochemical Approach to Understanding the Organization of the Olfactory System in the Cuttlefish, Sepia officinalis",

abstract = "Cephalopods are nontraditional but captivating models of invertebrate neurobiology, particularly in evolutionary comparisons. Cephalopod olfactory systems have striking similarities and fundamental differences with vertebrates, arthropods, and gastropods, raising questions about the ancestral origins of those systems. We describe here the organization and development of the olfactory system of the common cuttlefish, Sepia officinalis, using immunohistochemistry and in situ hybridization. FMRFamide and/or related peptides and histamine are putative neurotransmitters in olfactory sensory neurons. Other neurotransmitters, including serotonin and APGWamide within the olfactory and other brain lobes, suggest efferent control of olfactory input and/or roles in the processing of olfactory information. The distributions of neurotransmitters, along with staining patterns of phalloidin, anti-acetylated α-tubulin, and a synaptotagmin riboprobe, help to clarify the structure of the olfactory lobe. We discuss a key difference, the lack of identifiable olfactory glomeruli, in cuttlefish in comparison to other models, and suggest its implications for the evolution of olfaction.",

author = "Scaros, {Alexia T.} and Croll, {Roger P.} and S{\'e}bastien Baratte",

note = "Funding Information: *E-mail: baratte@mnhn.fr. ORCID Roger P. Croll: 0000-0002-9846-0923 Author Contributions The manuscript has been read and approved by all named authors, and there are no other persons who satisfied the criteria for authorship but are not listed. We further confirm that the order of authors listed in the manuscript has been approved by all of us. All authors had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Acquisition of data: A.T.S., S.B., and R.P.C. Analysis and interpretation of data: A.T.S., S.B., and R.P.C. Drafting of the manuscript: A.T.S., S.B., and R.P.C. Critical revision of the manuscript for important intellectual content: A.T.S., R.P.C., and S.B. Funding Natural Sciences and Engineering Research Council of Canada, Laboratoire Biologie des Organismes et Ecosysteḿ es Aqua-tiques in Paris (Le Centre National de la Recherche Scientifique, UMR 7208, Museum National d{\textquoteright}Histoire Nature-lle, Institut de Recherche pour le Developement France, 207, Universit{\'e} Pierre et Marie Curie), the France Canada Research Fund (2013), the Mitacs Globalink Research Program (2015), the province of Nova Scotia for the Graduate Scholarship (2017), and Dalhousie University for the International Differential Fee Scholarship (2017). Notes The authors declare no competing financial interest. Publisher Copyright: {\textcopyright} 2018 American Chemical Society.",

year = "2018",

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doi = "10.1021/acschemneuro.8b00021",

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AU - Scaros, Alexia T.

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N1 - Funding Information: *E-mail: baratte@mnhn.fr. ORCID Roger P. Croll: 0000-0002-9846-0923 Author Contributions The manuscript has been read and approved by all named authors, and there are no other persons who satisfied the criteria for authorship but are not listed. We further confirm that the order of authors listed in the manuscript has been approved by all of us. All authors had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Acquisition of data: A.T.S., S.B., and R.P.C. Analysis and interpretation of data: A.T.S., S.B., and R.P.C. Drafting of the manuscript: A.T.S., S.B., and R.P.C. Critical revision of the manuscript for important intellectual content: A.T.S., R.P.C., and S.B. Funding Natural Sciences and Engineering Research Council of Canada, Laboratoire Biologie des Organismes et Ecosysteḿ es Aqua-tiques in Paris (Le Centre National de la Recherche Scientifique, UMR 7208, Museum National d’Histoire Nature-lle, Institut de Recherche pour le Developement France, 207, Université Pierre et Marie Curie), the France Canada Research Fund (2013), the Mitacs Globalink Research Program (2015), the province of Nova Scotia for the Graduate Scholarship (2017), and Dalhousie University for the International Differential Fee Scholarship (2017). Notes The authors declare no competing financial interest. Publisher Copyright: © 2018 American Chemical Society.

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N2 - Cephalopods are nontraditional but captivating models of invertebrate neurobiology, particularly in evolutionary comparisons. Cephalopod olfactory systems have striking similarities and fundamental differences with vertebrates, arthropods, and gastropods, raising questions about the ancestral origins of those systems. We describe here the organization and development of the olfactory system of the common cuttlefish, Sepia officinalis, using immunohistochemistry and in situ hybridization. FMRFamide and/or related peptides and histamine are putative neurotransmitters in olfactory sensory neurons. Other neurotransmitters, including serotonin and APGWamide within the olfactory and other brain lobes, suggest efferent control of olfactory input and/or roles in the processing of olfactory information. The distributions of neurotransmitters, along with staining patterns of phalloidin, anti-acetylated α-tubulin, and a synaptotagmin riboprobe, help to clarify the structure of the olfactory lobe. We discuss a key difference, the lack of identifiable olfactory glomeruli, in cuttlefish in comparison to other models, and suggest its implications for the evolution of olfaction.

AB - Cephalopods are nontraditional but captivating models of invertebrate neurobiology, particularly in evolutionary comparisons. Cephalopod olfactory systems have striking similarities and fundamental differences with vertebrates, arthropods, and gastropods, raising questions about the ancestral origins of those systems. We describe here the organization and development of the olfactory system of the common cuttlefish, Sepia officinalis, using immunohistochemistry and in situ hybridization. FMRFamide and/or related peptides and histamine are putative neurotransmitters in olfactory sensory neurons. Other neurotransmitters, including serotonin and APGWamide within the olfactory and other brain lobes, suggest efferent control of olfactory input and/or roles in the processing of olfactory information. The distributions of neurotransmitters, along with staining patterns of phalloidin, anti-acetylated α-tubulin, and a synaptotagmin riboprobe, help to clarify the structure of the olfactory lobe. We discuss a key difference, the lack of identifiable olfactory glomeruli, in cuttlefish in comparison to other models, and suggest its implications for the evolution of olfaction.

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Immunohistochemical Approach to Understanding the Organization of the Olfactory System in the Cuttlefish, Sepia officinalis

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