Hunger signalling in the olfactory bulb primes exploration, food-seeking and peripheral metabolism

Stark, Romana; Dempsey, Harry; Kleeman, Elizabeth; Sassi, Martina; Osborne-Lawrence, Sherri; Sheybani-Deloui, Sepideh; Rushby, Helen J.; Mirth, Christen K.; Austin-Muttitt, Karl; Mullins, Jonathan; Zigman, Jeffrey M.; Davies, Jeffrey; Andrews, Zane B.

doi:10.1016/j.molmet.2024.102025

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Hunger signalling in the olfactory bulb primes exploration, food-seeking and peripheral metabolism

Romana Stark, Harry Dempsey, Elizabeth Kleeman, Martina Sassi, Sherri Osborne-Lawrence, Sepideh Sheybani-Deloui, Helen J. Rushby, Christen K. Mirth, Karl Austin-Muttitt, Jonathan Mullins

, Jeffrey M. Zigman, Jeffrey Davies

, Zane B. Andrews

Molecular Metabolism, Volume: 89, Start page: 102025

Swansea University Authors: Martina Sassi, Karl Austin-Muttitt, Jonathan Mullins , Jeffrey Davies

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DOI (Published version): 10.1016/j.molmet.2024.102025

Abstract

Objective Although the metabolic state of an organism affects olfactory function, the precise mechanisms and their impact on behavior and metabolism remain unknown. Here, we assess whether ghrelin receptors (GHSRs) in the olfactory bulb (OB) increase olfactory function and influence foraging behavio...

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Published in:	Molecular Metabolism
ISSN:	2212-8778 2212-8778
Published:	Elsevier BV 2024
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URI:	https://cronfa.swan.ac.uk/Record/cronfa67734
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Here, we assess whether ghrelin receptors (GHSRs) in the olfactory bulb (OB) increase olfactory function and influence foraging behaviors and metabolism. Methods We performed a detailed behavioural and metabolic analysis in mice lacking GHSRs in the OB (OBGHSR deletion). We also analsyed OB scRNA-seq and spatial transcriptomic datasets to assess GHSR+ cells in the main and accessory olfactory bulbs, as well as the anterior olfactory nucleus. Results OBGHSR deletion affected olfactory discrimination and habituation to both food and non-food odors. Anxiety-like and depression-like behaviors were significantly greater after OBGHSR deletion, whereas exploratory behavior was reduced, with the greatest effect under fasted conditions. OBGHSR deletion impacted feeding behavior as evidenced by altered bout number and duration, as well as buried food-seeking. OBGHSR deletion increased body weight and fat mass, spared fat utilisation on a chow diet and impaired glucose metabolism indicating metabolic dysfunction. Cross referenced analysis of OB scRNA-seq and spatial transcriptomic datasets revealed GHSR+ glutamate neurons in the main and accessory olfactory bulbs, as well as the anterior olfactory nucleus. Ablation of glutamate neurons in the OB reduced ghrelin-induced food finding and phenocopied results seen after OBGHSR deletion. Conclusions OBGHSRs help to maintain olfactory function, particularly during hunger, and facilitate behavioral adaptations that optimise food-seeking in anxiogenic environments, priming metabolic pathways in preparation for food consumption.</abstract><type>Journal Article</type><journal>Molecular Metabolism</journal><volume>89</volume><journalNumber/><paginationStart>102025</paginationStart><paginationEnd/><publisher>Elsevier BV</publisher><placeOfPublication/><isbnPrint/><isbnElectronic/><issnPrint>2212-8778</issnPrint><issnElectronic>2212-8778</issnElectronic><keywords>Hunger; Ghrelin; Anxiety; Metabolism; Olfaction; Glutamate; Olfactory bulb; Transcriptomics</keywords><publishedDay>1</publishedDay><publishedMonth>11</publishedMonth><publishedYear>2024</publishedYear><publishedDate>2024-11-01</publishedDate><doi>10.1016/j.molmet.2024.102025</doi><url/><notes/><college>COLLEGE NANME</college><CollegeCode>COLLEGE CODE</CollegeCode><institution>Swansea University</institution><apcterm>Another institution paid the OA fee</apcterm><funders>National Health and Medical Research Council of Australia APP1154974; APP1125960 (ZBA); APP1160065 (RS). Phenomics Australia is supported by the Australian Government Department of Education through the National Collaborative Research Infrastructure Strategy, the Super Science Initiative and the Collaborative Research Infrastructure Scheme.</funders><projectreference/><lastEdited>2024-10-21T17:06:23.2699613</lastEdited><Created>2024-09-19T13:03:03.6897763</Created><path><level id="1">Faculty of Medicine, Health and Life Sciences</level><level id="2">Swansea University Medical School - Biomedical Science</level></path><authors><author><firstname>Romana</firstname><surname>Stark</surname><order>1</order></author><author><firstname>Harry</firstname><surname>Dempsey</surname><order>2</order></author><author><firstname>Elizabeth</firstname><surname>Kleeman</surname><order>3</order></author><author><firstname>Martina</firstname><surname>Sassi</surname><order>4</order></author><author><firstname>Sherri</firstname><surname>Osborne-Lawrence</surname><order>5</order></author><author><firstname>Sepideh</firstname><surname>Sheybani-Deloui</surname><order>6</order></author><author><firstname>Helen J.</firstname><surname>Rushby</surname><order>7</order></author><author><firstname>Christen K.</firstname><surname>Mirth</surname><order>8</order></author><author><firstname>Karl</firstname><surname>Austin-Muttitt</surname><order>9</order></author><author><firstname>Jonathan</firstname><surname>Mullins</surname><orcid>0000-0003-0144-2962</orcid><order>10</order></author><author><firstname>Jeffrey M.</firstname><surname>Zigman</surname><order>11</order></author><author><firstname>Jeffrey</firstname><surname>Davies</surname><orcid>0000-0002-4234-0033</orcid><order>12</order></author><author><firstname>Zane B.</firstname><surname>Andrews</surname><orcid>0000-0002-9097-7944</orcid><order>13</order></author></authors><documents><document><filename>67734__32671__36815702e8394e7c93f9d68bd23d1344.pdf</filename><originalFilename>67734.VoR.pdf</originalFilename><uploaded>2024-10-21T17:05:23.1692673</uploaded><type>Output</type><contentLength>6781203</contentLength><contentType>application/pdf</contentType><version>Version of Record</version><cronfaStatus>true</cronfaStatus><documentNotes>2024 The Author(s). 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spelling	v2 67734 2024-09-19 Hunger signalling in the olfactory bulb primes exploration, food-seeking and peripheral metabolism 73844ea9bb96bff6f83ffeffa8f64a49 Martina Sassi Martina Sassi true false fafc0917b48af4eaec154646854867f8 Karl Austin-Muttitt Karl Austin-Muttitt true false 4cf2dddedbe1dacb506ec925fdbd5b40 0000-0003-0144-2962 Jonathan Mullins Jonathan Mullins true false 2cb3d1d96a7870a84d2f758e865172e6 0000-0002-4234-0033 Jeffrey Davies Jeffrey Davies true false 2024-09-19 Objective Although the metabolic state of an organism affects olfactory function, the precise mechanisms and their impact on behavior and metabolism remain unknown. Here, we assess whether ghrelin receptors (GHSRs) in the olfactory bulb (OB) increase olfactory function and influence foraging behaviors and metabolism. Methods We performed a detailed behavioural and metabolic analysis in mice lacking GHSRs in the OB (OBGHSR deletion). We also analsyed OB scRNA-seq and spatial transcriptomic datasets to assess GHSR+ cells in the main and accessory olfactory bulbs, as well as the anterior olfactory nucleus. Results OBGHSR deletion affected olfactory discrimination and habituation to both food and non-food odors. Anxiety-like and depression-like behaviors were significantly greater after OBGHSR deletion, whereas exploratory behavior was reduced, with the greatest effect under fasted conditions. OBGHSR deletion impacted feeding behavior as evidenced by altered bout number and duration, as well as buried food-seeking. OBGHSR deletion increased body weight and fat mass, spared fat utilisation on a chow diet and impaired glucose metabolism indicating metabolic dysfunction. Cross referenced analysis of OB scRNA-seq and spatial transcriptomic datasets revealed GHSR+ glutamate neurons in the main and accessory olfactory bulbs, as well as the anterior olfactory nucleus. Ablation of glutamate neurons in the OB reduced ghrelin-induced food finding and phenocopied results seen after OBGHSR deletion. Conclusions OBGHSRs help to maintain olfactory function, particularly during hunger, and facilitate behavioral adaptations that optimise food-seeking in anxiogenic environments, priming metabolic pathways in preparation for food consumption. Journal Article Molecular Metabolism 89 102025 Elsevier BV 2212-8778 2212-8778 Hunger; Ghrelin; Anxiety; Metabolism; Olfaction; Glutamate; Olfactory bulb; Transcriptomics 1 11 2024 2024-11-01 10.1016/j.molmet.2024.102025 COLLEGE NANME COLLEGE CODE Swansea University Another institution paid the OA fee National Health and Medical Research Council of Australia APP1154974; APP1125960 (ZBA); APP1160065 (RS). Phenomics Australia is supported by the Australian Government Department of Education through the National Collaborative Research Infrastructure Strategy, the Super Science Initiative and the Collaborative Research Infrastructure Scheme. 2024-10-21T17:06:23.2699613 2024-09-19T13:03:03.6897763 Faculty of Medicine, Health and Life Sciences Swansea University Medical School - Biomedical Science Romana Stark 1 Harry Dempsey 2 Elizabeth Kleeman 3 Martina Sassi 4 Sherri Osborne-Lawrence 5 Sepideh Sheybani-Deloui 6 Helen J. Rushby 7 Christen K. Mirth 8 Karl Austin-Muttitt 9 Jonathan Mullins 0000-0003-0144-2962 10 Jeffrey M. Zigman 11 Jeffrey Davies 0000-0002-4234-0033 12 Zane B. Andrews 0000-0002-9097-7944 13 67734__32671__36815702e8394e7c93f9d68bd23d1344.pdf 67734.VoR.pdf 2024-10-21T17:05:23.1692673 Output 6781203 application/pdf Version of Record true 2024 The Author(s). This is an open access article under the CC BY license. true eng http://creativecommons.org/licenses/by/4.0/
title	Hunger signalling in the olfactory bulb primes exploration, food-seeking and peripheral metabolism
spellingShingle	Hunger signalling in the olfactory bulb primes exploration, food-seeking and peripheral metabolism Martina Sassi Karl Austin-Muttitt Jonathan Mullins Jeffrey Davies
title_short	Hunger signalling in the olfactory bulb primes exploration, food-seeking and peripheral metabolism
title_full	Hunger signalling in the olfactory bulb primes exploration, food-seeking and peripheral metabolism
title_fullStr	Hunger signalling in the olfactory bulb primes exploration, food-seeking and peripheral metabolism
title_full_unstemmed	Hunger signalling in the olfactory bulb primes exploration, food-seeking and peripheral metabolism
title_sort	Hunger signalling in the olfactory bulb primes exploration, food-seeking and peripheral metabolism
author_id_str_mv	73844ea9bb96bff6f83ffeffa8f64a49 fafc0917b48af4eaec154646854867f8 4cf2dddedbe1dacb506ec925fdbd5b40 2cb3d1d96a7870a84d2f758e865172e6
author_id_fullname_str_mv	73844ea9bb96bff6f83ffeffa8f64a49_*_Martina Sassi fafc0917b48af4eaec154646854867f8__Karl Austin-Muttitt 4cf2dddedbe1dacb506ec925fdbd5b40__Jonathan Mullins 2cb3d1d96a7870a84d2f758e865172e6_*_Jeffrey Davies
author	Martina Sassi Karl Austin-Muttitt Jonathan Mullins Jeffrey Davies
author2	Romana Stark Harry Dempsey Elizabeth Kleeman Martina Sassi Sherri Osborne-Lawrence Sepideh Sheybani-Deloui Helen J. Rushby Christen K. Mirth Karl Austin-Muttitt Jonathan Mullins Jeffrey M. Zigman Jeffrey Davies Zane B. Andrews
format	Journal article
container_title	Molecular Metabolism
container_volume	89
container_start_page	102025
publishDate	2024
institution	Swansea University
issn	2212-8778 2212-8778
doi_str_mv	10.1016/j.molmet.2024.102025
publisher	Elsevier BV
college_str	Faculty of Medicine, Health and Life Sciences
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hierarchy_top_id	facultyofmedicinehealthandlifesciences
hierarchy_top_title	Faculty of Medicine, Health and Life Sciences
hierarchy_parent_id	facultyofmedicinehealthandlifesciences
hierarchy_parent_title	Faculty of Medicine, Health and Life Sciences
department_str	Swansea University Medical School - Biomedical Science{{{_:::_}}}Faculty of Medicine, Health and Life Sciences{{{_:::_}}}Swansea University Medical School - Biomedical Science
document_store_str	1
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description	Objective Although the metabolic state of an organism affects olfactory function, the precise mechanisms and their impact on behavior and metabolism remain unknown. Here, we assess whether ghrelin receptors (GHSRs) in the olfactory bulb (OB) increase olfactory function and influence foraging behaviors and metabolism. Methods We performed a detailed behavioural and metabolic analysis in mice lacking GHSRs in the OB (OBGHSR deletion). We also analsyed OB scRNA-seq and spatial transcriptomic datasets to assess GHSR+ cells in the main and accessory olfactory bulbs, as well as the anterior olfactory nucleus. Results OBGHSR deletion affected olfactory discrimination and habituation to both food and non-food odors. Anxiety-like and depression-like behaviors were significantly greater after OBGHSR deletion, whereas exploratory behavior was reduced, with the greatest effect under fasted conditions. OBGHSR deletion impacted feeding behavior as evidenced by altered bout number and duration, as well as buried food-seeking. OBGHSR deletion increased body weight and fat mass, spared fat utilisation on a chow diet and impaired glucose metabolism indicating metabolic dysfunction. Cross referenced analysis of OB scRNA-seq and spatial transcriptomic datasets revealed GHSR+ glutamate neurons in the main and accessory olfactory bulbs, as well as the anterior olfactory nucleus. Ablation of glutamate neurons in the OB reduced ghrelin-induced food finding and phenocopied results seen after OBGHSR deletion. Conclusions OBGHSRs help to maintain olfactory function, particularly during hunger, and facilitate behavioral adaptations that optimise food-seeking in anxiogenic environments, priming metabolic pathways in preparation for food consumption.
published_date	2024-11-01T17:06:21Z
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Hunger signalling in the olfactory bulb primes exploration, food-seeking and peripheral metabolism

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