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

Volumn 7, Issue 12, 2012, Pages

  Aimé, Pascaline ^a,d   Hegoburu, Chloé ^a   Jaillard, Tristan ^b   Degletagne, Cyril ^c   Garcia, Samuel ^a   Messaoudi, Belkacem ^a   Thevenet, Marc ^a   Lorsignol, Anne ^b   Duchamp, Claude ^c   Mouly, Anne Marie ^a   Julliard, Andrée Karyn ^a  

^a UNIVERSITÉ DE LYON   (France)

^b Institut National de la Sant é et de la Recherche Medicale   (France)

^c Laboratoire d'Ecologie des Hydrosystemes Naturels et Anthropises   (France)

^d NewYork Presbyterian Hospital   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN; INSULIN RECEPTOR;

ANALYSIS OF VARIANCE; ANIMAL EXPERIMENT; ARTICLE; AVERSION; AVERSIVE ODOR; BINDING SITE; BODY WEIGHT; CELL LABELING; CONDITIONED OLFACTORY AVERSION; CONTROLLED STUDY; ENZYME IMMUNOASSAY; FOOD INTAKE; GLUCOSE BLOOD LEVEL; HABITUATION; INFORMATION PROCESSING; INSULIN BLOOD LEVEL; INSULIN RELEASE; MALE; MITRAL CELL; NONHUMAN; ODOR; OLFACTORY BULB; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SATIETY; SNIFFING;

ANIMALS; AVOIDANCE LEARNING; BASE SEQUENCE; BEHAVIOR, ANIMAL; BLOOD GLUCOSE; DNA PRIMERS; FOOD; INJECTIONS, INTRAVENTRICULAR; INSULIN; MALE; ODORS; OLFACTORY BULB; RATS; RATS, WISTAR; SMELL;

ANIMALIA; RATTUS;

EID: 84871295159     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0051227     Document Type: Article

References (83)

1. Henquin JC, (2009) Regulation of insulin secretion: a matter of phase control and amplitude modulation. Diabetologia 52: 739-751.
2. Polonsky KS, Given BD, Van Cauter E, (1988) Twenty-four-hour profiles and pulsatile patterns of insulin secretion in normal and obese subjects. J Clin Invest 81: 442-448.
3. Saltiel AR, Kahn CR, (2001) Insulin signalling and the regulation of glucose and lipid metabolism. Nature 414: 799-806.
4. Frank HJ, Pardridge WM, Morris WL, Rosenfeld RG, Choi TB, (1986) Binding and internalization of insulin and insulin-like growth factors by isolated brain microvessels. Diabetes 35: 654-661.
5. Duffy KR, Pardridge WM, (1987) Blood-brain barrier transcytosis of insulin in developing rabbits. Brain Res 420: 32-38.
6. Schwartz MW, Sipols A, Kahn SE, Lattemann DF, Taborsky GJ Jr, et al. (1990) Kinetics and specificity of insulin uptake from plasma into cerebrospinal fluid. Am J Physiol 259: E378-383.
7. Banks WA, Jaspan JB, Kastin AJ, (1997) Selective, physiological transport of insulin across the blood-brain barrier: novel demonstration by species-specific radioimmunoassays. Peptides 18: 1257-1262.
8. Woods SC, Lotter EC, McKay LD, Porte D Jr, (1979) Chronic intracerebroventricular infusion of insulin reduces food intake and body weight of baboons. Nature 282: 503-505.
9. Brief DJ, Davis JD, (1984) Reduction of food intake and body weight by chronic intraventricular insulin infusion. Brain Res Bull 12: 571-575.
10. Plata-Salaman CR, Oomura Y, (1986) Effect of intra-third ventricular administration of insulin on food intake after food deprivation. Physiol Behav 37: 735-739.
11. Plata-Salaman CR, Oomura Y, Shimizu N, (1986) Dependence of food intake on acute and chronic ventricular administration of insulin. Physiol Behav 37: 717-734.
12. Jaillard T, Roger M, Galinier A, Guillou P, Benani A, et al. (2009) Hypothalamic reactive oxygen species are required for insulin-induced food intake inhibition: an NADPH oxidase-dependent mechanism. Diabetes 58: 1544-1549.
13. Air EL, Benoit SC, Blake Smith KA, Clegg DJ, Woods SC, (2002) Acute third ventricular administration of insulin decreases food intake in two paradigms. Pharmacol Biochem Behav 72: 423-429.
14. Bruning JC, Gautam D, Burks DJ, Gillette J, Schubert M, et al. (2000) Role of brain insulin receptor in control of body weight and reproduction. Science 289: 2122-2125.
15. Aime P, Duchamp-Viret P, Chaput MA, Savigner A, Mahfouz M, et al. (2007) Fasting increases and satiation decreases olfactory detection for a neutral odor in rats. Behav Brain Res 179: 258-264.
16. Prud'homme MJ, Lacroix MC, Badonnel K, Gougis S, Baly C, et al. (2009) Nutritional status modulates behavioural and olfactory bulb Fos responses to isoamyl acetate or food odour in rats: roles of orexins and leptin. Neuroscience 162: 1287-1298.
17. Pager J, Giachetti I, Holley A, Le Magnen J, (1972) A selective control of olfactory bulb electrical activity in relation to food deprivation and satiety in rats. Physiol Behav 9: 573-579.
18. Cain DP, (1975) Effects of insulin injection on responses of olfactory bulb and amygdala single units to odors. Brain Res 99: 69-83.
19. Chaput MA, Holley A, (1976) Olfactory bulb responsiveness to food odour during stomach distension in the rat. Chemical senses 2: 189-201.
20. Apelbaum AF, Chaput MA, (2003) Rats habituated to chronic feeding restriction show a smaller increase in olfactory bulb reactivity compared to newly fasted rats. Chem Senses 28: 389-395.
21. 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: 1127-1138.
22. Unger J, McNeill TH, Moxley RT 3rd, White M, Moss A, et al. (1989) Distribution of insulin receptor-like immunoreactivity in the rat forebrain. Neuroscience 31: 143-157.
23. Marks JL, Porte D Jr, Stahl WL, Baskin DG, (1990) Localization of insulin receptor mRNA in rat brain by in situ hybridization. Endocrinology 127: 3234-3236.
24. Marks JL, Eastman CJ, (1989) Effect of starvation on insulin receptors in rat brain. Neuroscience 30: 551-556.
25. Banks WA, Kastin AJ, Pan W, (1999) Uptake and degradation of blood-borne insulin by the olfactory bulb. Peptides 20: 373-378.
26. Baskin DG, Porte D Jr, Guest K, Dorsa DM, (1983) Regional concentrations of insulin in the rat brain. Endocrinology 112: 898-903.
27. 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: 6734-6751.
28. Wesson DW, Donahou TN, Johnson MO, Wachowiak M, (2008) Sniffing behavior of mice during performance in odor-guided tasks. Chem Senses 33: 581-596.
29. Monod B, Mouly AM, Vigouroux M, Holley A, (1989) An investigation of some temporal aspects of olfactory coding with the model of multi-site electrical stimulation of the olfactory bulb in the rat. Behav Brain Res 33: 51-63.
30. Hegoburu C, Shionoya K, Garcia S, Messaoudi B, Thevenet M, et al. (2011) The RUB Cage: Respiration-Ultrasonic Vocalizations-Behavior Acquisition Setup for Assessing Emotional Memory in Rats. Front Behav Neurosci 5: 25.
31. Mori K, (2003) Grouping of odorant receptors: odour maps in the mammalian olfactory bulb. Biochem Soc Trans 31: 134-136.
32. Mori K, Takahashi YK, Igarashi KM, Yamaguchi M, (2006) Maps of odorant molecular features in the Mammalian olfactory bulb. Physiol Rev 86: 409-433.
33. Julliard AK, Chaput MA, Apelbaum A, Aime P, Mahfouz M, et al. (2007) Changes in rat olfactory detection performance induced by orexin and leptin mimicking fasting and satiation. Behav Brain Res 183: 123-129.
34. 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: 1393-1401.
35. Delattre E, Cipolla-Neto J, Boschero AC, (1999) Diurnal variations in insulin secretion and K+ permeability in isolated rat islets. Clin Exp Pharmacol Physiol 26: 505-510.
36. Haj-ali V, Mohaddes G, Babri SH, (2009) Intracerebroventricular insulin improves spatial learning and memory in male Wistar rats. Behav Neurosci 123: 1309-1314.
37. Slotnick BM, Westbrook F, Darling FMC, (1997) What the rat's nose tells the rat's mouth: Long delay aversion conditioning with aqueous odors and potentiation of tatse by odors. Animal Learning & Behaviour 25: 357-369.
38. Mickley GA, Kenmuir CL, McMullen CA, Yocom AM, Valentine EL, et al. (2004) Dynamic processing of taste aversion extinction in the brain. Brain Res 1016: 79-89.
39. Sokal RR, Rohlf FJ (1981) Biometry: The Principals and Practice of Statistics in Biological Research San Francisco: Freeman, W.H. 859 p.
40. Julliard AK, Hartmann DJ, (1998) Spatiotemporal patterns of expression of extracellular matrix molecules in the developing and adult rat olfactory system. Neuroscience 84: 1135-1150.
41. Schwarzberg H, Bernstein HG, Reiser M, Gunther O, (1989) Intracerebroventricular administration of insulin attenuates retrieval of a passive avoidance response in rats. Neuropeptides 13: 79-81.
42. Park CR, Seeley RJ, Craft S, Woods SC, (2000) Intracerebroventricular insulin enhances memory in a passive-avoidance task. Physiol Behav 68: 509-514.
43. Park CR, (2001) Cognitive effects of insulin in the central nervous system. Neurosci Biobehav Rev 25: 311-323.
44. Youngentob SL, Mozell MM, Sheehe PR, Hornung DE, (1987) A quantitative analysis of sniffing strategies in rats performing odor detection tasks. Physiol Behav 41: 59-69.
45. Kepecs A, Uchida N, Mainen ZF, (2007) Rapid and precise control of sniffing during olfactory discrimination in rats. J Neurophysiol 98: 205-213.
46. Pager J, (1974) A selective modulation of olfactory input suppressed by lesions of the anterior limb of the anterior commisure. Physiol Behav 13: 523-526.
47. Ketterer C, Heni M, Thamer C, Herzberg-Schafer SA, Haring HU, et al. (2011) Acute, short-term hyperinsulinemia increases olfactory threshold in healthy subjects. Int J Obes (Lond) 35: 1135-1138.
48. Palouzier-Paulignan B, Lacroix MC, Aimé P, Baly C, Caillol M, et al. (2012) Olfaction under metabolic influences. Chem Senses 37: 769-97.
49. Macrides F, Eichenbaum HB, Forbes WB, (1982) Temporal relationship between sniffing and the limbic theta rhythm during odor discrimination reversal learning. J Neurosci 2: 1705-1717.
50. Welker WI, (1964) Analysis of sniffing in the albino rat. Behavior 22: 223-244.
51. Buonviso N, Amat C, Litaudon P, (2006) Respiratory modulation of olfactory neurons in the rodent brain. Chem Senses 31: 145-154.
52. Courtiol E, Hegoburu C, Litaudon P, Garcia S, Fourcaud-Trocme N, et al. (2011) Individual and synergistic effects of sniffing frequency and flow rate on olfactory bulb activity. J Neurophysiol 106: 2813-2824.
53. Rennaker RL, Chen CF, Ruyle AM, Sloan AM, Wilson DA, (2007) Spatial and temporal distribution of odorant-evoked activity in the piriform cortex. J Neurosci 27: 1534-1542.
54. Spors H, Wachowiak M, Cohen LB, Friedrich RW, (2006) Temporal dynamics and latency patterns of receptor neuron input to the olfactory bulb. J Neurosci 26: 1247-1259.
55. 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: 631-639.
56. Laing DG, (1983) Natural sniffing gives optimum odour perception for humans. Perception 12: 99-117.
57. Sobel N, Khan RM, Hartley CA, Sullivan EV, Gabrieli JD, (2000) Sniffing longer rather than stronger to maintain olfactory detection threshold. Chem Senses 25: 1-8.
58. Abraham NM, Spors H, Carleton A, Margrie TW, Kuner T, et al. (2004) Maintaining accuracy at the expense of speed: stimulus similarity defines odor discrimination time in mice. Neuron 44: 865-876.
59. Uchida N, Mainen ZF, (2003) Speed and accuracy of olfactory discrimination in the rat. Nat Neurosci 6: 1224-1229.
60. Wesson DW, Carey RM, Verhagen JV, Wachowiak M, (2008) Rapid encoding and perception of novel odors in the rat. PLoS Biol 6: e82.
61. Wesson DW, Verhagen JV, Wachowiak M, (2009) Why sniff fast? The relationship between sniff frequency, odor discrimination, and receptor neuron activation in the rat. J Neurophysiol 101: 1089-1102.
62. Tong J, Mannea E, Aime P, Pfluger PT, Yi CX, et al. (2011) Ghrelin enhances olfactory sensitivity and exploratory sniffing in rodents and humans. J Neurosci 31: 5841-5846.
63. Manin M, Balage M, Larue-Achagiotis C, Grizard J, (1988) Chronic intracerebroventricular infusion of insulin failed to alter brain insulin-binding sites, food intake, and body weight. J Neurochem 51: 1689-1695.
64. Lacroix MC, Badonnel K, Meunier N, Tan F, Schlegel-Le Poupon C, et al. (2008) Expression of insulin system in the olfactory epithelium: first approaches to its role and regulation. J Neuroendocrinol 20: 1176-1190.
65. Savigner A, Duchamp-Viret P, Grosmaitre X, Chaput M, Garcia S, et al. (2009) Modulation of spontaneous and odorant-evoked activity of rat olfactory sensory neurons by two anorectic peptides, insulin and leptin. J Neurophysiol 101: 2898-2906.
66. Bowlby MR, Fadool DA, Holmes TC, Levitan IB, (1997) Modulation of the Kv1.3 potassium channel by receptor tyrosine kinases. J Gen Physiol 110: 601-610.
67. Fadool DA, Levitan IB, (1998) Modulation of olfactory bulb neuron potassium current by tyrosine phosphorylation. J Neurosci 18: 6126-6137.
68. 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: 2332-2348.
69. Fadool DA, Tucker K, Perkins R, Fasciani G, Thompson RN, et al. (2004) Kv1.3 channel gene-targeted deletion produces "Super-Smeller Mice" with altered glomeruli, interacting scaffolding proteins, and biophysics. Neuron 41: 389-404.
70. Woods SC, Seeley RJ, Baskin DG, Schwartz MW, (2003) Insulin and the blood-brain barrier. Curr Pharm Des 9: 795-800.
71. Banks WA, (2004) The source of cerebral insulin. Eur J Pharmacol 490: 5-12.
72. Strubbe JH, Porte D Jr, Woods SC, (1988) Insulin responses and glucose levels in plasma and cerebrospinal fluid during fasting and refeeding in the rat. Physiol Behav 44: 205-208.
73. Woods SC, Porte D Jr, (1977) Relationship between plasma and cerebrospinal fluid insulin levels of dogs. Am J Physiol 233: E331-334.
74. Clegg DJ, Benoit SC, Reed JA, Woods SC, Dunn-Meynell A, et al. (2005) Reduced anorexic effects of insulin in obesity-prone rats fed a moderate-fat diet. Am J Physiol Regul Integr Comp Physiol 288: R981-986.
75. Shepherd GM, Chen WR, Willhite D, Migliore M, Greer CA, (2007) The olfactory granule cell: from classical enigma to central role in olfactory processing. Brain Res Rev 55: 373-382.
76. Matsumoto H, Rhoads DE, (1990) Specific binding of insulin to membranes from dendrodendritic synaptosomes of rat olfactory bulb. J Neurochem 54: 347-350.
77. 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: 411-423.
78. Johnson BA, Arguello S, Leon M, (2007) Odorants with multiple oxygen-containing functional groups and other odorants with high water solubility preferentially activate posterior olfactory bulb glomeruli. J Comp Neurol 502: 468-482.
79. Scott JW, Acevedo HP, Sherrill L, Phan M, (2007) Responses of the rat olfactory epithelium to retronasal air flow. J Neurophysiol 97: 1941-1950.
80. Burdach KJ, Kroeze JH, Koster EP, (1984) Nasal, retronasal, and gustatory perception: an experimental comparison. Percept Psychophys 36: 205-208.
81. Ruijschop RM, Boelrijk AE, de Graaf C, Westerterp-Plantenga MS, (2009) Retronasal aroma release and satiation: a review. J Agric Food Chem 57: 9888-9894.
82. Ruijschop RM, Burgering MJ, Jacobs MA, Boelrijk AE, (2009) Retro-nasal aroma release depends on both subject and product differences: a link to food intake regulation? Chem Senses 34: 395-403.
83. Ruijschop RM, Boelrijk AE, Burgering MJ, de Graaf C, Westerterp-Plantenga MS, (2010) Acute effects of complexity in aroma composition on satiation and food intake. Chem Senses 35: 91-100.