title: The way an odor is experienced during aversive conditioning determines the extent of the network recruited during retrieval: a multisite electrophysiological study in rats.
abstract: Recent findings have revealed the importance of orthonasal and retronasal olfaction in food memory, especially in conditioned odor aversion (COA); however, little is known about the dynamics of the cerebral circuit involved in the recognition of an odor as a toxic food signal and whether the activated network depends on the way (orthonasal vs retronasal) the odor was first experienced. In this study, we mapped the modulations of odor-induced oscillatory activities through COA learning using multisite recordings of local field potentials in behaving rats. During conditioning, orthonasal odor alone or associated with ingested odor was paired with immediate illness. For all animals, COA retrieval was assessed by orthonasal smelling only. Both types of conditioning induced similarly strong COA. Results pointed out (1) a predictive correlation between the emergence of powerful beta (15-40 Hz) activity and the behavioral expression of COA and (2) a differential network distribution of this beta activity according to the way the animals were exposed to the odor during conditioning. Indeed, for both types of conditioning, the aversive behavior was predicted by the emergence of a strong beta oscillatory activity in response to the odor in the olfactory bulb, piriform cortex, orbitofrontal cortex, and basolateral amygdala. This network was selectively extended to the infralimbic and insular cortices when the odor was ingested during acquisition. These differential networks could participate in different food odor memory; these results are discussed in line with recent behavioral results that indicate that COA can be formed over long odor-illness delays only if the odor is ingested.
authors.affiliation: Centre National de la Recherche Scientifique (CNRS) Unité Mixte de Recherche (UMR) 5020 Neurosciences Sensorielles Comportement Cognition, Université Lyon 1, Université de Lyon, Lyon, France. jchapuis@olfac.univ-lyon1.fr
authors.forename: Julie
authors.initials: J
authors.lastname: Chapuis
authors.forename: Samuel
authors.initials: S
authors.lastname: Garcia
authors.forename: Belkacem
authors.initials: B
authors.lastname: Messaoudi
authors.forename: Marc
authors.initials: M
authors.lastname: Thevenet
authors.forename: Guillaume
authors.initials: G
authors.lastname: Ferreira
authors.forename: Remi
authors.initials: R
authors.lastname: Gervais
authors.forename: Nadine
authors.initials: N
authors.lastname: Ravel
mesh_terms: D000200:Action Potentials / Q000502:physiology; D000818:Animals; D001362:Avoidance Learning / Q000502:physiology*; D003213:Conditioning, Psychological / Q000502:physiology*; D004567:Electrodes, Implanted; D008297:Male; D011939:Mental Recall / Q000502:physiology*; D009415:Nerve Net / Q000502:physiology*; D009812:Odorants; D051381:Rats; D017208:Rats, Wistar; D012903:Smell / Q000502:physiology*
references.citation: Eur J Neurosci. 2009 Apr;29(8):1654-62
references.pmid: 19419428
references.citation: Physiol Behav. 1985 Jan;34(1):71-7
references.pmid: 4034697
references.citation: J Neurosci. 2008 Jun 25;28(26):6664-9
references.pmid: 18579740
references.citation: Trends Cogn Sci. 2001 Jan 1;5(1):16-25
references.pmid: 11164732
references.citation: Nat Rev Neurosci. 2001 Apr;2(4):229-39
references.pmid: 11283746
references.citation: J Neurosci. 2008 Mar 12;28(11):2864-73
references.pmid: 18337417
references.citation: Brain Res Bull. 1996;41(6):391-8
references.pmid: 8973845
references.citation: Brain Res. 2005 Jul 27;1051(1-2):176-82
references.pmid: 15961067
references.citation: Neuron. 2005 Aug 18;47(4):593-605
references.pmid: 16102541
references.citation: Neurobiol Learn Mem. 1997 Jan;67(1):80-3
references.pmid: 9013505
references.citation: Cereb Cortex. 2007 Jun;17(6):1342-9
references.pmid: 16882682
references.citation: Trends Cogn Sci. 1999 Apr;3(4):151-162
references.pmid: 10322469
references.citation: J Neurophysiol. 2007 Oct;98(4):2196-205
references.pmid: 17699692
references.citation: Neurobiol Learn Mem. 2007 May;87(4):659-68
references.pmid: 17223581
references.citation: Biol Psychiatry. 2007 Nov 15;62(10):1070-9
references.pmid: 17826749
references.citation: J Comp Physiol Psychol. 1976 Jan;90(1):67-77
references.pmid: 965515
references.citation: Chem Senses. 2005 Oct;30(8):693-706
references.pmid: 16177226
references.citation: Brain Res Bull. 2000 Dec;53(6):751-8
references.pmid: 11179839
references.citation: J Neurosci Methods. 2007 Feb 15;160(1):135-43
references.pmid: 17049617
references.citation: J Comp Physiol Psychol. 1982 Aug;96(4):540-8
references.pmid: 6288779
references.citation: J Neurosci. 2007 Aug 1;27(31):8358-65
references.pmid: 17670982
references.citation: Proc Natl Acad Sci U S A. 2008 Mar 18;105(11):4399-404
references.pmid: 18334648
references.citation: Brain Res. 2008 Oct 21;1236:166-75
references.pmid: 18725214
references.citation: J Neurosci Methods. 1980 Dec;3(2):129-49
references.pmid: 6110810
references.citation: J Physiol Paris. 2004 Jul-Nov;98(4-6):467-78
references.pmid: 16274975
references.citation: Behav Neurosci. 1996 Aug;110(4):760-5
references.pmid: 8864267
references.citation: Learn Mem. 2006 May-Jun;13(3):254-8
references.pmid: 16741279
references.citation: Brain Res Bull. 1984 Mar;12(3):221-6
references.pmid: 6722597
references.citation: Eur J Neurosci. 2006 Apr;23(7):1801-10
references.pmid: 16623837
references.citation: J Comp Neurol. 2005 Jul 25;488(2):224-31
references.pmid: 15924345
references.citation: Trends Neurosci. 1989 Jul;12(7):258-64
references.pmid: 2475938
references.citation: Neuroreport. 2004 Aug 6;15(11):1837-41
references.pmid: 15257158
references.citation: Learn Mem. 2008 Aug 26;15(9):649-56
references.pmid: 18772252
references.citation: J Neurosci. 2004 Jan 14;24(2):389-97
references.pmid: 14724237
references.citation: Learn Mem. 2004 Jul-Aug;11(4):453-8
references.pmid: 15254217
references.citation: Percept Psychophys. 1982 Apr;31(4):397-401
references.pmid: 7110896
references.citation: Nat Rev Neurosci. 2004 Mar;5(3):209-17
references.pmid: 14976520
references.citation: Learn Mem. 2007 Sep 06;14(9):616-24
references.pmid: 17848501
references.citation: J Neurosci. 1994 Sep;14(9):5437-52
references.pmid: 8083747
references.citation: Neurosci Res. 1990 Dec;9(3):196-201
references.pmid: 1963677
references.citation: J Comp Neurol. 1988 Apr 1;270(1):39-54, 62-3
references.pmid: 2453537
references.citation: Eur J Neurosci. 2005 Nov;22(10):2596-604
references.pmid: 16307602
references.citation: Behav Neurosci. 2006 Jun;120(3):590-9
references.pmid: 16768611
references.citation: Behav Neurosci. 2007 Dec;121(6):1383-92
references.pmid: 18085892
references.citation: J Neurosci. 2005 Sep 28;25(39):8903-7
references.pmid: 16192380
references.citation: Eur J Neurosci. 2008 Mar;27(6):1432-40
references.pmid: 18364022
references.citation: J Comp Neurol. 1998 Oct 5;399(4):440-68
references.pmid: 9741477
references.citation: J Neurophysiol. 1998 Jan;79(1):21-36
references.pmid: 9425173
references.citation: Neurosci Biobehav Rev. 2001 Jul;25(5):395-407
references.pmid: 11566478
references.citation: Learn Mem. 2006 Mar-Apr;13(2):150-60
references.pmid: 16547160
references.citation: J Neurosci. 1999 Mar 1;19(5):1876-84
references.pmid: 10024371
references.citation: J Neurosci. 2007 Mar 14;27(11):2858-65
references.pmid: 17360907
references.citation: Physiol Behav. 1986 Oct;38(4):503-8
references.pmid: 3823162
references.citation: Chem Senses. 1996 Oct;21(5):529-43
references.pmid: 8902282
references.citation: Behav Neurosci. 2006 Dec;120(6):1257-67
references.pmid: 17201470
references.citation: Physiol Behav. 1974 Feb;12(2):189-95
references.pmid: 4816076
references.citation: Neurobiol Learn Mem. 2007 Sep;88(2):186-97
references.pmid: 17531515
references.citation: Ann N Y Acad Sci. 2007 Dec;1121:136-51
references.pmid: 17846155
references.citation: Learn Mem. 2009 Mar 20;16(4):235-42
references.pmid: 19304894
references.citation: Eur J Neurosci. 2003 Nov;18(9):2605-10
references.pmid: 14622162
references.citation: J Comp Neurol. 2004 Aug 30;476(4):414-28
references.pmid: 15282713
references.citation: Eur J Neurosci. 2003 Jan;17(2):350-8
references.pmid: 12542672