Chronic restricted access to food leading to undernutrition affects rat neuroendocrine status and olfactory-driven behaviors

Hormones and Behavior

Volumn 62, Issue 2, 2012, Pages 120-127

  Badonnel, Karine ^a,b   Lacroix, Marie Christine ^a,b   Monnerie, Régine ^a,b   Durieux, Didier ^a,b   Caillol, Monique ^a,b   Baly, Christine ^a,b  

^a INRA   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

Behavior; Food intake; Insulin; Leptin; Neuroendocrine status; Olfaction

Indexed keywords

GLUCOSE; INSULIN; INSULIN RECEPTOR; LEPTIN; LEPTIN RECEPTOR; TRIACYLGLYCEROL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CONTROLLED STUDY; DIET RESTRICTION; FOOD INTAKE; GENETIC TRANSCRIPTION; GLUCOSE BLOOD LEVEL; HORMONE BLOOD LEVEL; INSULIN BLOOD LEVEL; MALE; MALNUTRITION; NEUROENDOCRINE SYSTEM; NONHUMAN; NUCLEOTIDE SEQUENCE; ODOR; OLFACTORY BULB; OLFACTORY EPITHELIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SMELLING; TRIACYLGLYCEROL BLOOD LEVEL; WEIGHT REDUCTION;

ANIMALS; BEHAVIOR, ANIMAL; BODY WEIGHT; CALORIC RESTRICTION; EATING; FEEDING BEHAVIOR; FOOD DEPRIVATION; MALE; MALNUTRITION; NEUROSECRETORY SYSTEMS; RATS; RATS, WISTAR; RECEPTOR, INSULIN; RECEPTORS, LEPTIN; SMELL; TIME FACTORS;

EID: 84864321110     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2012.05.010     Document Type: Article

References (45)

1. Aime P., Duchamp-Viret P., Chaput M.A., Savigner A., Mahfouz M., Julliard A.K. Fasting increases and satiation decreases olfactory detection for a neutral odor in rats. Behav. Brain. Res. 2007, 179:258-264.
2. Albrecht J., Schreder T., Kleemann A.M., Schopf V., Kopietz R., Anzinger A., Demmel M., Linn J., Kettenmann B., Wiesmann M. Olfactory detection thresholds and pleasantness of a food-related and a non-food odour in hunger and satiety. Rhinology 2009, 47:160-165.
3. Baly C., Aioun J., Badonnel K., Lacroix M.C., Durieux D., Schlegel C., Salesse R., Caillol M. Leptin and its receptors are present in the rat olfactory mucosa and modulated by the nutritional status. Brain Res. 2007, 1129:130-141.
4. Bi S., Robinson B.M., Moran T.H. Acute food deprivation and chronic food restriction differentially affect hypothalamic NPY mRNA expression. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2003, 285:R1030-R1036.
5. Cabanac M., Fantino M. Origin of olfacto-gustatory alliesthesia: intestinal sensitivity to carbohydrate concentration?. Physiol. Behav. 1977, 18:1039-1045.
6. Caillol M., Aioun J., Baly C., Persuy M.A., Salesse R. Localization of orexins and their receptors in the rat olfactory system: possible modulation of olfactory perception by a neuropeptide synthetized centrally or locally. Brain Res. 2003, 960:48-61.
7. Cain D.P. Effects of insulin injection on responses of olfactory bulb and amygdala single units to odors. Brain Res. 1975, 99:69-83.
8. Cameron J.D., Goldfield G.S., Cyr M.J., Doucet E. The effects of prolonged caloric restriction leading to weight-loss on food hedonics and reinforcement. Physiol. Behav. 2008, 94:474-480.
9. Challet E., Mendoza J. Metabolic and reward feeding synchronises the rhythmic brain. Cell Tissue Res. 2010, 341:1-11.
10. Chiba T., Yamaza H., Higami Y., Shimokawa I. Anti-aging effects of caloric restriction: involvement of neuroendocrine adaptation by peripheral signaling. Microsc. Res. Tech. 2002, 59:317-324.
11. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 1987, 162:156-159.
12. Cuesta M., Clesse D., Pevet P., Challet E. From daily behavior to hormonal and neurotransmitters rhythms: comparison between diurnal and nocturnal rat species. Horm. Behav. 2009, 55:338-347.
13. Fadool D.A., Tucker K., Phillips J.J., Simmen J.A. Brain insulin receptor causes activity-dependent current suppression in the olfactory bulb through multiple phosphorylation of Kv1.3. J. Neurophysiol. 2000, 83:2332-2348.
14. Feillet C.A. Food for thoughts: feeding time and hormonal secretion. J. Neuroendocrinol. 2010, 22:620-628.
15. Getchell T.V., Kwong K., Saunders C.P., Stromberg A.J., Getchell M.L. Leptin regulates olfactory-mediated behavior in ob/ob mice. Physiol. Behav. 2006, 87:848-856.
16. Gunapala K.M., Gallardo C.M., Hsu C.T., Steele A.D. Single gene deletions of orexin, leptin, neuropeptide Y, and ghrelin do not appreciably alter food anticipatory activity in mice. PLoS One 2011, 6:e18377.
17. Havel P.J. Peripheral signals conveying metabolic information to the brain: short-term and long-term regulation of food intake and energy homeostasis. Exp. Biol. Med. (Maywood) 2001, 226:963-977.
18. Jiang T., Soussignan R., Rigaud D., Martin S., Royet J.P., Brondel L., Schaal B. Alliesthesia to food cues: heterogeneity across stimuli and sensory modalities. Physiol. Behav. 2008, 95:464-470.
19. Johansson A., Fredriksson R., Winnergren S., Hulting A.L., Schioth H.B., Lindblom J. The relative impact of chronic food restriction and acute food deprivation on plasma hormone levels and hypothalamic neuropeptide expression. Peptides 2008, 29:1588-1595.
20. Julliard A.K., Chaput M.A., Apelbaum A., Aime P., Mahfouz M., Duchamp-Viret P. Changes in rat olfactory detection performance induced by orexin and leptin mimicking fasting and satiation. Behav. Brain Res. 2007, 183:123-129.
21. Kalsbeek A., Yi C.X., La Fleur S.E., Fliers E. The hypothalamic clock and its control of glucose homeostasis. Trends Endocrinol. Metab. 2010, 21:402-410.
22. Ketterer C., Heni M., Thamer C., Herzberg-Schafer S.A., Haring H.U., Fritsche A. Acute, short-term hyperinsulinemia increases olfactory threshold in healthy subjects. Int. J. Obes. (Lond.) 2011, 35:1135-1138.
23. Lacroix M.C., Badonnel K., Meunier N., Tan F., Schlegel-Le Poupon C., Durieux D., Monnerie R., Baly C., Congar P., Salesse R., Caillol M. Expression of insulin system in the olfactory epithelium: first approaches to its role and regulation. J. Neuroendocrinol. 2008, 20:1176-1190.
24. Le Pichon C.E., Valley M.T., Polymenidou M., Chesler A.T., Sagdullaev B.T., Aguzzi A., Firestein S. Olfactory behavior and physiology are disrupted in prion protein knockout mice. Nat. Neurosci. 2009, 12:60-69.
25. Lecoultre V., Ravussin E., Redman L.M. The fall in leptin concentration is a major determinant of the metabolic adaptation induced by caloric restriction independently of the changes in leptin circadian rhythms. J. Clin. Endocrinol. Metab. 2011, 96:E1512-E1516.
26. Mattson M.P., Duan W., Guo Z. Meal size and frequency affect neuronal plasticity and vulnerability to disease: cellular and molecular mechanisms. J. Neurochem. 2003, 84:417-431.
27. Mistlberger R.E. Circadian food-anticipatory activity: formal models and physiological mechanisms. Neurosci. Biobehav. Rev. 1994, 18:171-195.
28. Moran T.H., Ladenheim E.E. Adiposity signaling and meal size control. Physiol. Behav. 2011, 103:21-24.
29. Poulin A.M., Timofeeva E. The dynamics of neuronal activation during food anticipation and feeding in the brain of food-entrained rats. Brain Res. 2008, 1227:128-141.
30. Prud'homme M.J., Lacroix M.C., Badonnel K., Gougis S., Baly C., Salesse R., Caillol M. Nutritional status modulates behavioural and olfactory bulb Fos responses to isoamyl acetate or food odour in rats: roles of orexins and leptin. Neuroscience 2009, 162:1287-1298.
31. Redman L.M., Ravussin E. Endocrine alterations in response to calorie restriction in humans. Mol. Cell. Endocrinol. 2009, 299:129-136.
32. Redman L.M., Ravussin E. Caloric restriction in humans: impact on physiological, psychological, and behavioral outcomes. Antioxid. Redox Signal. 2011, 14:275-287.
33. Rowland N.E., Vaughan C.H., Mathes C.M., Mitra A. Feeding behavior, obesity, and neuroeconomics. Physiol. Behav. 2008, 93:97-109.
34. Saito H., Mimmack M., Kishimoto J., Keverne E.B., Emson P.C. Expression of olfactory receptors, G-proteins and AxCAMs during the development and maturation of olfactory sensory neurons in the mouse. Brain Res. Dev. Brain Res. 1998, 110:69-81.
35. Saladin R., De Vos P., Guerre-Millo M., Leturque A., Girard J., Staels B., Auwerx J. Transient increase in obese gene expression after food intake or insulin administration. Nature 1995, 377:527-529.
36. Savigner A., Duchamp-Viret P., Grosmaitre X., Chaput M., Garcia S., Ma M., Palouzier-Paulignan B. Modulation of spontaneous and odorant-evoked activity of rat olfactory sensory neurons by two anorectic peptides, insulin and leptin. J. Neurophysiol. 2009, 101:2898-2906.
37. Schloegl H., Percik R., Horstmann A., Villringer A., Stumvoll M. Peptide hormones regulating appetite-focus on neuroimaging studies in humans. Diabetes Metab. Res. Rev. 2011, 27:104-112.
38. Shizgal P., Fulton S., Woodside B. Brain reward circuitry and the regulation of energy balance. Int. J. Obes. Relat. Metab. Disord. 2001, 25(Suppl. 5):S17-S21.
39. Silver R., Balsam P. Oscillators entrained by food and the emergence of anticipatory timing behaviors. Sleep Biol. Rhythms 2010, 8:120-136.
40. Stafford L.D., Welbeck K. High hunger state increases olfactory sensitivity to neutral but not food odors. Chem. Senses 2011, 36:189-198.
41. Stephan F.K. The "other" circadian system: food as a Zeitgeber. J. Biol. Rhythms 2002, 17:284-292.
42. Sucajtys-Szulc E., Turyn J., Goyke E., Korczynska J., Stelmanska E., Slominska E., Smolenski R.T., Rutkowski B., Swierczynski J. Differential effect of prolonged food restriction and fasting on hypothalamic malonyl-CoA concentration and expression of orexigenic and anorexigenic neuropeptides genes in rats. Neuropeptides 2010, 44:17-23.
43. Tong J., Mannea E., Aime P., Pfluger P.T., Yi C.X., Castaneda T.R., Davis H.W., Ren X., Pixley S., Benoit S., Julliard K., Woods S.C., Horvath T.L., Sleeman M.M., D'Alessio D., Obici S., Frank R., Tschop M.H. Ghrelin enhances olfactory sensitivity and exploratory sniffing in rodents and humans. J. Neurosci. 2011, 31:5841-5846.
44. Trellakis S., Tagay S., Fischer C., Rydleuskaya A., Scherag A., Bruderek K., Schlegl S., Greve J., Canbay A.E., Lang S., Brandau S. Ghrelin, leptin and adiponectin as possible predictors of the hedonic value of odors. Regul. Pept. 2011, 167:112-117.
45. Wachowiak M. All in a sniff: olfaction as a model for active sensing. Neuron 2011, 71:962-973.