Advertisement

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 Julliard
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.

References

  1. Aime P, Duchamp-Viret P, Chaput MA, Savigner A, Mahfouz M, Julliard AK (2007) Fasting increases and satiation decreases olfactory detection for a neutral odor in rats. Behav Brain Res 179(2):258–264.  https://doi.org/10.1016/j.bbr.2007.02.012 CrossRefPubMedGoogle Scholar
  2. Aime P, Hegoburu C, Jaillard T, Degletagne C, Garcia S, Messaoudi B, Thevenet M, Lorsignol A, Duchamp C, Mouly AM, Julliard AK (2012) A physiological increase of insulin in the olfactory bulb decreases detection of a learned aversive odor and abolishes food odor-induced sniffing behavior in rats. PLoS One 7(12):e51227.  https://doi.org/10.1371/journal.pone.0051227 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Aime P, Palouzier-Paulignan B, Salem R, Al Koborssy D, Garcia S, Duchamp C, Romestaing C, Julliard AK (2014) Modulation of olfactory sensitivity and glucose-sensing by the feeding state in obese Zucker rats. Front Behav Neurosci 8:326.  https://doi.org/10.3389/fnbeh.2014.00326 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Ainscow EK, Mirshamsi S, Tang T, Ashford ML, Rutter GA (2002) Dynamic imaging of free cytosolic ATP concentration during fuel sensing by rat hypothalamic neurones: evidence for ATP-independent control of ATP-sensitive K(+) channels. J Physiol 544(Pt 2):429–445CrossRefGoogle Scholar
  5. Al Koborssy D, Palouzier-Paulignan B, Salem R, Thevenet M, Romestaing C, Julliard AK (2014) Cellular and molecular cues of glucose sensing in the rat olfactory bulb. Front Neurosci 8:333.  https://doi.org/10.3389/fnins.2014.00333 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Anand BK, Chhina GS, Sharma KN, Dua S, Singh B (1964) Activity of single neurons in the hypothalamic feeding centers: effect of glucose. Am J Physiol 207:1146–1154PubMedGoogle Scholar
  7. Ashrafi G, Wu Z, Farrell RJ, Ryan TA (2017) GLUT4 mobilization supports energetic demands of active synapses. Neuron 93(3):606–615 e603.  https://doi.org/10.1016/j.neuron.2016.12.020 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Balfour RH, Hansen AM, Trapp S (2006) Neuronal responses to transient hypoglycaemia in the dorsal vagal complex of the rat brainstem. J Physiol 570(Pt 3):469–484.  https://doi.org/10.1113/jphysiol.2005.098822 CrossRefPubMedGoogle Scholar
  9. Banks WA, Kastin AJ, Pan W (1999) Uptake and degradation of blood-borne insulin by the olfactory bulb. Peptides 20(3):373–378CrossRefGoogle Scholar
  10. Barnes DC, Hofacer RD, Zaman AR, Rennaker RL, Wilson DA (2008) Olfactory perceptual stability and discrimination. Nat Neurosci 11(12):1378–1380.  https://doi.org/10.1038/nn.2217 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Baskin DG, Porte D, Guest K, Dorsa DM (1983) Regional concentrations of insulin in the rat brain. Endocrinology 112(3):898–903CrossRefGoogle Scholar
  12. Bathellier B, Buhl DL, Accolla R, Carleton A (2008) Dynamic ensemble odor coding in the mammalian olfactory bulb: sensory information at different timescales. Neuron 57(4):586–598.  https://doi.org/10.1016/j.neuron.2008.02.011 CrossRefPubMedGoogle Scholar
  13. Bignami A, Eng LF, Dahl D, Uyeda CT (1972) Localization of the glial fibrillary acidic protein in astrocytes by immunofluorescence. Brain Res 43(2):429–435CrossRefGoogle Scholar
  14. Blevins JE, Truong BG, Gietzen DW (2004) NMDA receptor function within the anterior piriform cortex and lateral hypothalamus in rats on the control of intake of amino acid-deficient diets. Brain Res 1019(1–2):124–133.  https://doi.org/10.1016/j.brainres.2004.05.089 CrossRefPubMedGoogle Scholar
  15. Burdakov D (2007) K + channels stimulated by glucose: a new energy-sensing pathway. Pflugers Arch 454(1):19–27.  https://doi.org/10.1007/s00424-006-0189-8 CrossRefPubMedGoogle Scholar
  16. Burdakov D, Lesage F (2010) Glucose-induced inhibition: how many ionic mechanisms? Acta Physiol (Oxf) 198(3):295–301.  https://doi.org/10.1111/j.1748-1716.2009.02005.x CrossRefGoogle Scholar
  17. Carnevali L, Sgoifo A, Trombini M, Landgraf R, Neumann ID, Nalivaiko E (2013) Different patterns of respiration in rat lines selectively bred for high or low anxiety. PLoS One 8(5):e64519.  https://doi.org/10.1371/journal.pone.0064519 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Cayabyab FS, Khanna R, Jones OT, Schlichter LC (2000) Suppression of the rat microglia Kv1.3 current by src-family tyrosine kinases and oxygen/glucose deprivation. Eur J Neurosci 12(6):1949–1960CrossRefGoogle Scholar
  19. Chapuis J, Wilson DA (2011) Bidirectional plasticity of cortical pattern recognition and behavioral sensory acuity. Nat Neurosci 15(1):155–161.  https://doi.org/10.1038/nn.2966 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Cleland TA, Morse A, Yue EL, Linster C (2002) Behavioral models of odor similarity. Behav Neurosci 116(2):222–231CrossRefGoogle Scholar
  21. Cohen-Matsliah SI, Rosenblum K, Barkai E (2009) Olfactory-learning abilities are correlated with the rate by which intrinsic neuronal excitability is modulated in the piriform cortex. Eur J Neurosci 30(7):1339–1348.  https://doi.org/10.1111/j.1460-9568.2009.06894.x CrossRefPubMedGoogle Scholar
  22. Colley BS, Biju KC, Visegrady A, Campbell S, Fadool DA (2007) Neurotrophin B receptor kinase increases Kv subfamily member 1.3 (Kv1.3) ion channel half-life and surface expression. Neuroscience 144(2):531–546.  https://doi.org/10.1016/j.neuroscience.2006.09.055 CrossRefPubMedGoogle Scholar
  23. Coronas-Samano G, Ivanova AV, Verhagen JV (2016) The habituation/cross-habituation test revisited: guidance from sniffing and video tracking. Neural Plast 2016:9131284.  https://doi.org/10.1155/2016/9131284 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Cotero VE, Routh VH (2009) Insulin blunts the response of glucose-excited neurons in the ventrolateral-ventromedial hypothalamic nucleus to decreased glucose. Am J Physiol Endocrinol Metab 296(5):E1101–E1109.  https://doi.org/10.1152/ajpendo.90932.2008 CrossRefPubMedPubMedCentralGoogle Scholar
  25. De Rosa E, Hasselmo ME (2000) Muscarinic cholinergic neuromodulation reduces proactive interference between stored odor memories during associative learning in rats. Behav Neurosci 114(1):32–41CrossRefGoogle Scholar
  26. Demattè ML, Endrizzi I, Biasioli F, Corollaro ML, Pojer N, Zampini M, Aprea E, Gasperi F (2013) Food neophobia and its relation with olfactory ability in common odour identification. Appetite 68:112–117.  https://doi.org/10.1016/j.appet.2013.04.021 CrossRefPubMedGoogle Scholar
  27. Djukic B, Casper KB, Philpot BD, Chin LS, McCarthy KD (2007) Conditional knock-out of Kir4.1 leads to glial membrane depolarization, inhibition of potassium and glutamate uptake, and enhanced short-term synaptic potentiation. J Neurosci 27(42):11354–11365.  https://doi.org/10.1523/JNEUROSCI.0723-07.2007 CrossRefPubMedGoogle Scholar
  28. Dunn-Meynell AA, Routh VH, Kang L, Gaspers L, Levin BE (2002) Glucokinase is the likely mediator of glucosensing in both glucose-excited and glucose-inhibited central neurons. Diabetes 51(7):2056–2065CrossRefGoogle Scholar
  29. Ekstrand JJ, Domroese ME, Johnson DM, Feig SL, Knodel SM, Behan M, Haberly LB (2001) A new subdivision of anterior piriform cortex and associated deep nucleus with novel features of interest for olfaction and epilepsy. J Comp Neurol 434(3):289–307CrossRefGoogle Scholar
  30. El Messari S, Ait-Ikhlef A, Ambroise DH, Penicaud L, Arluison M (2002) Expression of insulin-responsive glucose transporter GLUT4 mRNA in the rat brain and spinal cord: an in situ hybridization study. J Chem Neuroanat 24(4):225–242. (S0891061802000583 [pii])CrossRefGoogle Scholar
  31. Eng LF, Vanderhaeghen JJ, Bignami A, Gerstl B (1971) An acidic protein isolated from fibrous astrocytes. Brain Res 28(2):351–354CrossRefGoogle Scholar
  32. Fadool DA, Levitan IB (1998) Modulation of olfactory bulb neuron potassium current by tyrosine phosphorylation. J Neurosci 18(16):6126–6137CrossRefGoogle Scholar
  33. Fadool DA, Tucker K, Phillips JJ, Simmen JA (2000) Brain insulin receptor causes activity-dependent current suppression in the olfactory bulb through multiple phosphorylation of Kv1.3. J Neurophysiol 83(4):2332–2348CrossRefGoogle Scholar
  34. Fadool DA, Tucker K, Perkins R, Fasciani G, Thompson RN, Parsons AD, Overton JM, Koni PA, Flavell RA, Kaczmarek LK (2004) Kv1.3 channel gene-targeted deletion produces “Super-Smeller Mice” with altered glomeruli, interacting scaffolding proteins, and biophysics. Neuron 41(3):389–404. (S0896627303008444 [pii])CrossRefGoogle Scholar
  35. Fadool DA, Tucker K, Pedarzani P (2011) Mitral cells of the olfactory bulb perform metabolic sensing and are disrupted by obesity at the level of the Kv1.3 ion channel. PLoS One 6(9):e24921.  https://doi.org/10.1371/journal.pone.0024921 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Fletcher M, Wilson DA (2001) Ontogeny of odor discrimination: a method to assess novel odor discrimination in neonatal rats. Physiol Behav 74(4–5):589–593CrossRefGoogle Scholar
  37. Franks KM, Isaacson JS (2005) Synapse-specific downregulation of NMDA receptors by early experience: a critical period for plasticity of sensory input to olfactory cortex. Neuron 47(1):101–114.  https://doi.org/10.1016/j.neuron.2005.05.024 CrossRefPubMedGoogle Scholar
  38. Garcia S, Fourcaud-Trocme N (2009) OpenElectrophy: an electrophysiological data- and analysis-sharing framework. Front Neuroinform 3:14.  https://doi.org/10.3389/neuro.11.014.2009 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Gibb AJ, Edwards FA (1994) Patch clamp recording from cells in sliced tissues. In: Microelectrode Techniques. The Plymouth Workshop Handbook, CambridgeGoogle Scholar
  40. Grundy D (2015) Principles and standards for reporting animal experiments in The Journal of Physiology and Experimental Physiology. J Physiol 593(12):2547–2549.  https://doi.org/10.1113/JP270818 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Haberly LB (1983) Structure of the piriform cortex of the opossum. I. Description of neuron types with Golgi methods. J Comp Neurol 213(2):163–187.  https://doi.org/10.1002/cne.902130205 CrossRefPubMedGoogle Scholar
  42. Haberly LB (2001) Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. Chem Senses 26(5):551–576CrossRefGoogle Scholar
  43. Hegoburu C, Shionoya K, Garcia S, Messaoudi B, Thevenet M, Mouly AM (2011) The RUB cage: respiration–ultrasonic vocalizations–behavior acquisition setup for assessing emotional memory in rats. Front Behav Neurosci 5:25.  https://doi.org/10.3389/fnbeh.2011.00025 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Hill JM, Lesniak MA, Pert CB, Roth J (1986) Autoradiographic localization of insulin receptors in rat brain: prominence in olfactory and limbic areas. Neuroscience 17(4):1127–1138CrossRefGoogle Scholar
  45. Julliard AK, Hartmann DJ (1998) Spatiotemporal patterns of expression of extracellular matrix molecules in the developing and adult rat olfactory system. Neuroscience 84(4):1135–1150CrossRefGoogle Scholar
  46. Julliard A, Chaput M, Apelbaum A, Aime P, Mahfouz M, Duchamp-Viret P (2007) Changes in rat olfactory detection performance induced by orexin and leptin mimicking fasting and satiation. Behav Brain Res 183(2):123–129CrossRefGoogle Scholar
  47. Julliard AK, Al Koborssy D, Fadool DA, Palouzier-Paulignan B (2017) Nutrient sensing: another chemosensitivity of the olfactory system. Front Physiol 8:468.  https://doi.org/10.3389/fphys.2017.00468 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Kapur A, Lytton WW, Ketchum KL, Haberly LB (1997) Regulation of the NMDA component of EPSPs by different components of postsynaptic GABAergic inhibition: computer simulation analysis in piriform cortex. J Neurophysiol 78(5):2546–2559.  https://doi.org/10.1152/jn.1997.78.5.2546 CrossRefPubMedGoogle Scholar
  49. Karschin C, Ecke C, Ashcroft FM, Karschin A (1997) Overlapping distribution of K(ATP) channel-forming Kir6.2 subunit and the sulfonylurea receptor SUR1 in rodent brain. FEBS Lett 401(1):59–64CrossRefGoogle Scholar
  50. Kaul L, Berdanier CD (1975) Effect of meal-feeding on the daily variations of insulin, glucose, and NADP-linked dehydrogenases in rats. J Nutr 105(9):1132–1140CrossRefGoogle Scholar
  51. Kepecs A, Uchida N, Mainen ZF (2007) Rapid and precise control of sniffing during olfactory discrimination in rats. J Neurophysiol 98(1):205–213.  https://doi.org/10.1152/jn.00071.2007 CrossRefPubMedGoogle Scholar
  52. Kobayashi M, Nikami H, Morimatsu M, Saito M (1996) Expression and localization of insulin-regulatable glucose transporter (GLUT4) in rat brain. Neurosci Lett 213(2):103–106CrossRefGoogle Scholar
  53. Kovach CP, Al Koborssy D, Huang Z, Chelette BM, Fadool JM, Fadool DA (2016) Mitochondrial ultrastructure and glucose signaling pathways attributed to the Kv1.3 Ion channel. Front Physiol 7:178.  https://doi.org/10.3389/fphys.2016.00178 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Krimer LS, Goldman-Rakic PS (1997) An interface holding chamber for anatomical and physiological studies of living brain slices. J Neurosci Methods 75(1):55–58CrossRefGoogle Scholar
  55. Kuczewski N, Fourcaud-Trocme N, Savigner A, Thevenet M, Aime P, Garcia S, Duchamp-Viret P, Palouzier-Paulignan B (2014) Insulin modulates network activity in olfactory bulb slices: impact on odour processing. J Physiol 592(13):2751–2769.  https://doi.org/10.1113/jphysiol.2013.269639 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Kues WA, Wunder F (1992) Heterogeneous expression patterns of mammalian potassium channel genes in developing and adult rat brain. Eur J Neurosci 4(12):1296–1308CrossRefGoogle Scholar
  57. Lacroix MC, Caillol M, Durieux D, Monnerie R, Grebert D, Pellerin L, Repond C, Tolle V, Zizzari P, Baly C (2015) Long-lasting metabolic imbalance related to obesity alters olfactory tissue homeostasis and impairs olfactory-driven behaviors. Chem Senses 40(8):537–556.  https://doi.org/10.1093/chemse/bjv039 CrossRefPubMedGoogle Scholar
  58. Leto D, Saltiel AR (2012) Regulation of glucose transport by insulin: traffic control of GLUT4. Nat Rev Mol Cell Biol 13(6):383–396.  https://doi.org/10.1038/nrm3351 CrossRefGoogle Scholar
  59. Li Y, Wang P, Xu J, Desir GV (2006) Voltage-gated potassium channel Kv1.3 regulates GLUT4 trafficking to the plasma membrane via a Ca2+-dependent mechanism. Am J Physiol Cell Physiol 290(2):C345–C351.  https://doi.org/10.1152/ajpcell.00091.2005 CrossRefPubMedGoogle Scholar
  60. Linster C, Hasselmo ME (2001) Neuromodulation and the functional dynamics of piriform cortex. Chem Senses 26(5):585–594CrossRefGoogle Scholar
  61. Macrides F, Eichenbaum HB, Forbes WB (1982) Temporal relationship between sniffing and the limbic theta rhythm during odor discrimination reversal learning. J Neurosci 2(12):1705–1717CrossRefGoogle Scholar
  62. Marks JL, Porte D, Stahl WL, Baskin DG (1990) Localization of insulin receptor mRNA in rat brain by in situ hybridization. Endocrinology 127(6):3234–3236.  https://doi.org/10.1210/endo-127-6-3234 CrossRefPubMedGoogle Scholar
  63. Marks DR, Tucker K, Cavallin MA, Mast TG, Fadool DA (2009) Awake intranasal insulin delivery modifies protein complexes and alters memory, anxiety, and olfactory behaviors. J Neurosci 29(20):6734–6751.  https://doi.org/10.1523/JNEUROSCI.1350-09.2009 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Marty N, Dallaporta M, Thorens B (2007) Brain glucose sensing, counterregulation, and energy homeostasis. Physiology (Bethesda) 22:241–251.  https://doi.org/10.1152/physiol.00010.2007 CrossRefGoogle Scholar
  65. McNay EC, Cotero VE (2010) Mini-review: impact of recurrent hypoglycemia on cognitive and brain function. Physiol Behav 100(3):234–238.  https://doi.org/10.1016/j.physbeh.2010.01.004 CrossRefPubMedPubMedCentralGoogle Scholar
  66. McNay EC, Recknagel AK (2011) Brain insulin signaling: a key component of cognitive processes and a potential basis for cognitive impairment in type 2 diabetes. Neurobiol Learn Mem 96(3):432–442.  https://doi.org/10.1016/j.nlm.2011.08.005 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Moriyama R, Tsukamura H, Kinoshita M, Okazaki H, Kato Y, Maeda K (2004) In vitro increase in intracellular calcium concentrations induced by low or high extracellular glucose levels in ependymocytes and serotonergic neurons of the rat lower brainstem. Endocrinology 145(5):2507–2515.  https://doi.org/10.1210/en.2003-1191 CrossRefPubMedGoogle Scholar
  68. Oomura Y, Ono T, Ooyama H, Wayner MJ (1969) Glucose and osmosensitive neurones of the rat hypothalamus. Nature 222(5190):282–284CrossRefGoogle Scholar
  69. Palouzier-Paulignan B, Lacroix MC, Aime P, Baly C, Caillol M, Congar P, Julliard AK, Tucker K, Fadool DA (2012) Olfaction under metabolic influences. Chem Senses 37(9):769–797.  https://doi.org/10.1093/chemse/bjs059 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Paxinos G, Watson C (2013) The rat brain in stereotaxic coordinates, 7th edn. Academic Press, San DiegoGoogle Scholar
  71. Pearson-Leary J, McNay EC (2016) Novel roles for the insulin-regulated glucose transporter-4 in hippocampally dependent memory. J Neurosci 36(47):11851–11864.  https://doi.org/10.1523/JNEUROSCI.1700-16.2016 CrossRefPubMedPubMedCentralGoogle Scholar
  72. Price JL (1973) An autoradiographic study of complementary laminar patterns of termination of afferent fibers to the olfactory cortex. J Comp Neurol 150(1):87–108.  https://doi.org/10.1002/cne.901500105 CrossRefPubMedGoogle Scholar
  73. Price JL, Sprich WW (1975) Observations on the lateral olfactory tract of the rat. J Comp Neurol 162(3):321–336.  https://doi.org/10.1002/cne.901620304 CrossRefPubMedGoogle Scholar
  74. Ranade S, Hangya B, Kepecs A (2013) Multiple modes of phase locking between sniffing and whisking during active exploration. J Neurosci 33(19):8250–8256.  https://doi.org/10.1523/JNEUROSCI.3874-12.2013 CrossRefPubMedPubMedCentralGoogle Scholar
  75. Rankin CH, Abrams T, Barry RJ, Bhatnagar S, Clayton DF, Colombo J, Coppola G, Geyer MA, Glanzman DL, Marsland S, McSweeney FK, Wilson DA, Wu CF, Thompson RF (2009) Habituation revisited: an updated and revised description of the behavioral characteristics of habituation. Neurobiol Learn Mem 92(2):135–138.  https://doi.org/10.1016/j.nlm.2008.09.012 CrossRefPubMedGoogle Scholar
  76. Ren X, Zhou L, Terwilliger R, Newton SS, de Araujo IE (2009) Sweet taste signaling functions as a hypothalamic glucose sensor. Front Integr Neurosci 3:12.  https://doi.org/10.3389/neuro.07.012.2009 CrossRefPubMedPubMedCentralGoogle Scholar
  77. Riera CE, Tsaousidou E, Halloran J, Follett P, Hahn O, Pereira MMA, Ruud LE, Alber J, Tharp K, Anderson CM, Bronneke H, Hampel B, Filho CDM, Stahl A, Bruning JC, Dillin A (2017) The Sense of Smell Impacts Metabolic Health and Obesity. Cell Metab 26(1):198–211 e195.  https://doi.org/10.1016/j.cmet.2017.06.015 CrossRefPubMedGoogle Scholar
  78. Rojas-Libano D, Kay LM (2012) Interplay between sniffing and odorant sorptive properties in the rat. J Neurosci 32(44):15577–15589.  https://doi.org/10.1523/JNEUROSCI.1464-12.2012 CrossRefPubMedPubMedCentralGoogle Scholar
  79. Rojas-Libano D, Frederick DE, Egana JI, Kay LM (2014) The olfactory bulb theta rhythm follows all frequencies of diaphragmatic respiration in the freely behaving rat. Front Behav Neurosci 8:214.  https://doi.org/10.3389/fnbeh.2014.00214 CrossRefPubMedPubMedCentralGoogle Scholar
  80. Rudell JB, Rechs AJ, Kelman TJ, Ross-Inta CM, Hao S, Gietzen DW (2011) The anterior piriform cortex is sufficient for detecting depletion of an indispensable amino acid, showing independent cortical sensory function. J Neurosci 31(5):1583–1590.  https://doi.org/10.1523/JNEUROSCI.4934-10.2011 CrossRefPubMedPubMedCentralGoogle Scholar
  81. Sachse S, Beshel J (2016) The good, the bad, and the hungry: how the central brain codes odor valence to facilitate food approach in Drosophila. Curr Opin Neurobiol 40:53–58.  https://doi.org/10.1016/j.conb.2016.06.012 CrossRefPubMedPubMedCentralGoogle Scholar
  82. Schoenbaum G, Eichenbaum H (1995) Information coding in the rodent prefrontal cortex. I. Single-neuron activity in orbitofrontal cortex compared with that in pyriform cortex. J Neurophysiol 74(2):733–750.  https://doi.org/10.1152/jn.1995.74.2.733 CrossRefPubMedGoogle Scholar
  83. Schulingkamp RJ, Pagano TC, Hung D, Raffa RB (2000) Insulin receptors and insulin action in the brain: review and clinical implications. Neurosci Biobehav Rev 24(8):855–872CrossRefGoogle Scholar
  84. Shepherd GM (2004) The synaptic organization of the brain, 5th edn. Oxford University Press, Oxford; New YorkCrossRefGoogle Scholar
  85. Sibille J, Pannasch U, Rouach N (2014) Astroglial potassium clearance contributes to short-term plasticity of synaptically evoked currents at the tripartite synapse. J Physiol 592(1):87–102.  https://doi.org/10.1113/jphysiol.2013.261735 CrossRefPubMedGoogle Scholar
  86. Sitren HS, Stevenson NR (1978) The effects of meal-feeding at different times of the day on daily changes in serum insulin, gastrin and liver enzymes in the rat. J Nutr 108(9):1393–1401CrossRefGoogle Scholar
  87. Staubli U, Schottler F, Nejat-Bina D (1987) Role of dorsomedial thalamic nucleus and piriform cortex in processing olfactory information. Behav Brain Res 25(2):117–129CrossRefGoogle Scholar
  88. Stockli J, Fazakerley DJ, James DE (2011) GLUT4 exocytosis. J Cell Sci 124(Pt 24):4147–4159.  https://doi.org/10.1242/jcs.097063 CrossRefPubMedPubMedCentralGoogle Scholar
  89. Sundberg H, Doving K, Novikov S, Ursin H (1982) A method for studying responses and habituation to odors in rats. Behav Neural Biol 34(1):113–119CrossRefGoogle Scholar
  90. Suzuki N, Bekkers JM (2006) Neural coding by two classes of principal cells in the mouse piriform cortex. J Neurosci 26(46):11938–11947.  https://doi.org/10.1523/JNEUROSCI.3473-06.2006 CrossRefPubMedGoogle Scholar
  91. Suzuki N, Bekkers JM (2010) Inhibitory neurons in the anterior piriform cortex of the mouse: classification using molecular markers. J Comp Neurol 518(10):1670–1687.  https://doi.org/10.1002/cne.22295 CrossRefPubMedGoogle Scholar
  92. Thiebaud N, Johnson MC, Butler JL, Bell GA, Ferguson KL, Fadool AR, Fadool JC, Gale AM, Gale DS, Fadool DA (2014) Hyperlipidemic diet causes loss of olfactory sensory neurons, reduces olfactory discrimination, and disrupts odor-reversal learning. J Neurosci 34(20):6970–6984.  https://doi.org/10.1523/JNEUROSCI.3366-13.2014 CrossRefPubMedPubMedCentralGoogle Scholar
  93. Tucker K, Cho S, Thiebaud N, Henderson MX, Fadool DA (2013) Glucose sensitivity of mouse olfactory bulb neurons is conveyed by a voltage-gated potassium channel. J Physiol 591(Pt 10):2541–2561.  https://doi.org/10.1113/jphysiol.2013.254086 CrossRefPubMedPubMedCentralGoogle Scholar
  94. Uchida N, Mainen ZF (2003) Speed and accuracy of olfactory discrimination in the rat. Nat Neurosci 6(11):1224–1229.  https://doi.org/10.1038/nn1142 CrossRefPubMedGoogle Scholar
  95. Unger J, McNeill TH, Moxley RT, White M, Moss A, Livingston JN (1989) Distribution of insulin receptor-like immunoreactivity in the rat forebrain. Neuroscience 31(1):143–157CrossRefGoogle Scholar
  96. Venner A, Karnani MM, Gonzalez JA, Jensen LT, Fugger L, Burdakov D (2011) Orexin neurons as conditional glucosensors: paradoxical regulation of sugar sensing by intracellular fuels. J Physiol 589(Pt 23):5701–5708.  https://doi.org/10.1113/jphysiol.2011.217000 CrossRefPubMedPubMedCentralGoogle Scholar
  97. Verhagen JV, Wesson DW, Netoff TI, White JA, Wachowiak M (2007) Sniffing controls an adaptive filter of sensory input to the olfactory bulb. Nat Neurosci 10(5):631–639.  https://doi.org/10.1038/nn1892 CrossRefPubMedGoogle Scholar
  98. Wachowiak M, Shipley MT (2006) Coding and synaptic processing of sensory information in the glomerular layer of the olfactory bulb. Semin Cell Dev Biol 17(4):411–423.  https://doi.org/10.1016/j.semcdb.2006.04.007 CrossRefPubMedGoogle Scholar
  99. Wada A, Yokoo H, Yanagita T, Kobayashi H (2005) New twist on neuronal insulin receptor signaling in health, disease, and therapeutics. J Pharmacol Sci 99(2):128–143CrossRefGoogle Scholar
  100. Welker WI (1964) Analysis of sniffing of the albino rat. Behaviour 22(3–4):223–244CrossRefGoogle Scholar
  101. Wesson DW, Keller M, Douhard Q, Baum MJ, Bakker J (2006) Enhanced urinary odor discrimination in female aromatase knockout (ArKO) mice. Horm Behav 49(5):580–586.  https://doi.org/10.1016/j.yhbeh.2005.12.013 CrossRefPubMedPubMedCentralGoogle Scholar
  102. Wesson DW, Donahou TN, Johnson MO, Wachowiak M (2008) Sniffing behavior of mice during performance in odor-guided tasks. Chem Senses 33(7):581–596.  https://doi.org/10.1093/chemse/bjn029 CrossRefPubMedPubMedCentralGoogle Scholar
  103. Wesson DW, Varga-Wesson AG, Borkowski AH, Wilson DA (2011) Respiratory and sniffing behaviors throughout adulthood and aging in mice. Behav Brain Res 223(1):99–106.  https://doi.org/10.1016/j.bbr.2011.04.016 CrossRefPubMedPubMedCentralGoogle Scholar
  104. Wilson DA (2000) Odor specificity of habituation in the rat anterior piriform cortex. J Neurophysiol 83(1):139–145.  https://doi.org/10.1152/jn.2000.83.1.139 CrossRefPubMedGoogle Scholar
  105. Wilson DA (2003) Rapid, experience-induced enhancement in odorant discrimination by anterior piriform cortex neurons. J Neurophysiol 90(1):65–72.  https://doi.org/10.1152/jn.00133.2003 CrossRefPubMedGoogle Scholar
  106. Wilson DA (2009a) Olfaction as a model system for the neurobiology of mammalian short-term habituation. Neurobiol Learn Mem 92(2):199–205.  https://doi.org/10.1016/j.nlm.2008.07.010 CrossRefPubMedGoogle Scholar
  107. Wilson DA (2009b) Pattern separation and completion in olfaction. Ann N Y Acad Sci 1170:306–312.  https://doi.org/10.1111/j.1749-6632.2009.04017.x CrossRefPubMedPubMedCentralGoogle Scholar
  108. Wilson DA, Stevenson RJ (2003) The fundamental role of memory in olfactory perception. Trends Neurosci 26(5):243–247.  https://doi.org/10.1016/S0166-2236(03)00076-6 CrossRefPubMedGoogle Scholar
  109. Wilson DA, Sullivan RM (2011) Cortical processing of odor objects. Neuron 72(4):506–519.  https://doi.org/10.1016/j.neuron.2011.10.027 CrossRefPubMedPubMedCentralGoogle Scholar
  110. Xu J, Wang P, Li Y, Li G, Kaczmarek LK, Wu Y, Koni PA, Flavell RA, Desir GV (2004) The voltage-gated potassium channel Kv1.3 regulates peripheral insulin sensitivity. Proc Natl Acad Sci USA 101(9):3112–3117.  https://doi.org/10.1073/pnas.0308450100 CrossRefPubMedGoogle Scholar
  111. Youngentob SL (2005) A method for the rapid automated assessment of olfactory function. Chem Senses 30(3):219–229.  https://doi.org/10.1093/chemse/bji017 CrossRefPubMedPubMedCentralGoogle Scholar
  112. Youngentob SL, Mozell MM, Sheehe PR, Hornung DE (1987) A quantitative analysis of sniffing strategies in rats performing odor detection tasks. Physiol Behav 41(1):59–69CrossRefGoogle Scholar
  113. Zhou Y, Wang X, Cao T, Xu J, Wang D, Restrepo D, Li A (2017) Insulin modulates neural activity of pyramidal neurons in the anterior piriform cortex. Front Cell Neurosci 11:378.  https://doi.org/10.3389/fncel.2017.00378 CrossRefPubMedPubMedCentralGoogle Scholar

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

Personalised recommendations