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Brain Structure and Function

, Volume 224, Issue 1, pp 315–336 | Cite as

Modulation of olfactory-driven behavior by metabolic signals: role of the piriform cortex

  • Dolly Al Koborssy
  • Brigitte Palouzier-Paulignan
  • Vincent Canova
  • Marc Thevenet
  • Debra Ann Fadool
  • Andrée Karyn JulliardEmail author
Original Article

Abstract

Olfaction is one of the major sensory modalities that regulates food consumption and is in turn regulated by the feeding state. Given that the olfactory bulb has been shown to be a metabolic sensor, we explored whether the anterior piriform cortex (aPCtx)—a higher olfactory cortical processing area—had the same capacity. Using immunocytochemical approaches, we report the localization of Kv1.3 channel, glucose transporter type 4, and the insulin receptor in the lateral olfactory tract and Layers II and III of the aPCtx. In current-clamped superficial pyramidal (SP) cells, we report the presence of two populations of SP cells: glucose responsive and non-glucose responsive. Using varied glucose concentrations and a glycolysis inhibitor, we found that insulin modulation of the instantaneous and spike firing frequency are both glucose dependent and require glucose metabolism. Using a plethysmograph to record sniffing frequency, rats microinjected with insulin failed to discriminate ratiometric enantiomers; considered a difficult task. Microinjection of glucose prevented discrimination of odorants of different chain-lengths, whereas injection of margatoxin increased the rate of habituation to repeated odor stimulation and enhanced discrimination. These data suggest that metabolic signaling pathways that are present in the aPCtx are capable of neuronal modulation and changing complex olfactory behaviors in higher olfactory centers.

Keywords

Olfaction Piriform Glucose GLUT4 Insulin Kv1.3 Sniffing behavior 

Notes

Acknowledgements

We would like to thank Ounsa Ben Hellal, Wesley Joshua Earl, and Abigail Thomas for routine technical assistance and rat husbandry.

Funding

This work was supported by the Centre National de la Recherche Scientifique, University Lyon 1, the Laboratoire d’Excellence Cortex (ANR-11-LABX-0042), and the National Institutes of Health (NIH) R01 DC013080 from the National Institutes of Deafness and Communication Disorders (NIDCD). The collaboration was supported by a PALSE grant (Programme Avenir Lyon Saint-Etienne) from the University of Lyon 1; the Robert B. Short Zoology Scholarship, the Brenda Weems Bennison Endowment, and the Pasquale Graziadei Endowment Fund from The Florida State University.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Research involving animals and ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. Experimental protocols were approved by the Lyon University Animal Experimentation Committee, the French Ministry of Higher Education and Research (APAFIS#9924-20170051614351992 v1), and the Florida State University (FSU) Institutional Animal Care and Use Committee (IACUC) under protocols no. 1427 and 1733. Experiments were carried out in accordance with the European Community Council Directive of November 24, 1986 (86/609/EEC), the American Veterinary Medicine Association (AVMA), and the National Institutes of Health (NIH).

Informed consent

This article does not contain any studies with human participants performed by any of the authors.

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Program in NeuroscienceThe Florida State UniversityTallahasseeUSA
  2. 2.Univ Lyon, Université Claude Bernard Lyon1, Centre de Recherche en Neurosciences de Lyon (CRNL), INSERM U1028/CNRS UMR5292 Team Olfaction: From Coding to MemoryLyonFrance
  3. 3.Institute of Molecular BiophysicsThe Florida State UniversityTallahasseeUSA
  4. 4.Department of Biological ScienceThe Florida State UniversityTallahasseeUSA

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