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

被引:47
作者
Aime, Pascaline [1 ,5 ]
Hegoburu, Chloe [1 ]
Jaillard, Tristan [2 ,3 ]
Degletagne, Cyril [4 ]
Garcia, Samuel [1 ]
Messaoudi, Belkacem [1 ]
Thevenet, Marc [1 ]
Lorsignol, Anne [2 ,3 ]
Duchamp, Claude [4 ]
Mouly, Anne-Marie [1 ]
Julliard, Andree Karyn [1 ]
机构
[1] Univ Lyon 1, Ctr Rech Neurosci Lyon, Team Olfact,CNRS UMR 5292, INSERM U1028, F-69365 Lyon, France
[2] Univ Toulouse 3, CNRS UMR 5241, F-31062 Toulouse, France
[3] Univ Toulouse 3, CNRS UMR 5273, INSERM, EFS,U1031,STROMALab, F-31062 Toulouse, France
[4] Univ Lyon 1, CNRS UMR 5023, LEHNA, F-69622 Villeurbanne, France
[5] Columbia Univ, Dept Pathol & Cell Biol, Med Ctr, New York, NY USA
关键词
BLOOD-BRAIN-BARRIER; CHRONIC INTRACEREBROVENTRICULAR INFUSION; BODY-WEIGHT; CEREBROSPINAL-FLUID; EVOKED ACTIVITY; RECEPTOR; MODULATION; DISCRIMINATION; RESPONSES; SECRETION;
D O I
10.1371/journal.pone.0051227
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
070301 [无机化学]; 070403 [天体物理学]; 070507 [自然资源与国土空间规划学]; 090105 [作物生产系统与生态工程];
摘要
Insulin is involved in multiple regulatory mechanisms, including body weight and food intake, and plays a critical role in metabolic disorders such as obesity and diabetes. An increasing body of evidence indicates that insulin is also involved in the modulation of olfactory function. The olfactory bulb (OB) contains the highest level of insulin and insulin receptors (IRs) in the brain. However, a role for insulin in odor detection and sniffing behavior remains to be elucidated. Using a behavioral paradigm based on conditioned olfactory aversion (COA) to isoamyl-acetate odor, we demonstrated that an intracerebroventricular (ICV) injection of 14 mU insulin acutely decreased olfactory detection of fasted rats to the level observed in satiated animals. In addition, whereas fasted animals demonstrated an increase in respiratory frequency upon food odor detection, this effect was absent in fasted animals receiving a 14 mU insulin ICV injection as well as in satiated animals. In parallel, we showed that the OB and plasma insulin levels were increased in satiated rats compared to fasted rats, and that a 14 mU insulin ICV injection elevated the OB insulin level of fasted rats to that of satiated rats. We further quantified insulin receptors (IRs) distribution and showed that IRs are preferentially expressed in the caudal and lateral parts of the main OB, with the highest labeling found in the mitral cells, the main OB projection neurons. Together, these data suggest that insulin acts on the OB network to modulate olfactory processing and demonstrate that olfactory function is under the control of signals involved in energy homeostasis regulation and feeding behaviors. Citation: Aime P, Hegoburu C, Jaillard T, Degletagne C, Garcia S, et al. (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. doi:10.1371/journal.pone.0051227
引用
收藏
页数:13
相关论文
共 83 条
[1]
Abraham NM, 2004, NEURON, V44, P865, DOI 10.1016/j.neuron.2004.11.017
[2]
Fasting increases and satiation decreases olfactory detection for a neutral odor in rats [J].
Aime, P. ;
Duchamp-Viret, P. ;
Chaput, M. A. ;
Savigner, A. ;
Mahfouz, M. ;
Julliard, A. K. .
BEHAVIOURAL BRAIN RESEARCH, 2007, 179 (02) :258-264
[3]
Acute third ventricular administration of insulin decreases food intake in two paradigms [J].
Air, EL ;
Benoit, SC ;
Smith, KAB ;
Clegg, DJ ;
Woods, SC .
PHARMACOLOGY BIOCHEMISTRY AND BEHAVIOR, 2002, 72 (1-2) :423-429
[4]
Rats habituated to chronic feeding restriction show a smaller increase in olfactory bulb reactivity compared to newly fasted rats [J].
Apelbaum, AF ;
Chaput, MA .
CHEMICAL SENSES, 2003, 28 (05) :389-395
[5]
Selective, physiological transport of insulin across the blood-brain barrier: Novel demonstration by species-specific radioimmunoassays [J].
Banks, WA ;
Jaspan, JB ;
Kastin, AJ .
PEPTIDES, 1997, 18 (08) :1257-1262
[6]
The source of cerebral insulin [J].
Banks, WA .
EUROPEAN JOURNAL OF PHARMACOLOGY, 2004, 490 (1-3) :5-12
[7]
Uptake and degradation of blood-borne insulin by the olfactory bulb [J].
Banks, WA ;
Kastin, AJ ;
Pan, WH .
PEPTIDES, 1999, 20 (03) :373-378
[8]
REGIONAL CONCENTRATIONS OF INSULIN IN THE RAT-BRAIN [J].
BASKIN, DG ;
PORTE, D ;
GUEST, K ;
DORSA, DM .
ENDOCRINOLOGY, 1983, 112 (03) :898-903
[9]
Modulation of the Kv1.3 potassium channel by receptor tyrosine kinases [J].
Bowlby, MR ;
Fadool, DA ;
Holmes, TC ;
Levitan, IB .
JOURNAL OF GENERAL PHYSIOLOGY, 1997, 110 (05) :601-610
[10]
REDUCTION OF FOOD-INTAKE AND BODY-WEIGHT BY CHRONIC INTRAVENTRICULAR INSULIN INFUSION [J].
BRIEF, DJ ;
DAVIS, JD .
BRAIN RESEARCH BULLETIN, 1984, 12 (05) :571-575