Neonatal odor-shock conditioning alters the neural network involved in odor fear learning at adulthood.
Adult learning and memory functions are strongly dependent on neonatal experiences. We recently showed that neonatal odor-shock learning attenuates later life odor fear conditioning and amygdala activity. In the present work we investigated whether changes observed in adults can also be observed in other structures normally involved, namely olfactory cortical areas. For this, pups were trained daily from postnatal (PN) 8 to 12 in an odor-shock paradigm, and retrained at adulthood in the same task. (14)C 2-DG autoradiographic brain mapping was used to measure training-related activation in amygdala cortical nucleus (CoA), anterior (aPCx), and posterior (pPCx) piriform cortex. In addition, field potentials induced in the three sites in response to paired-pulse stimulation of the olfactory bulb were recorded in order to assess short-term inhibition and facilitation in these structures. Attenuated adult fear learning was accompanied by a deficit in 2-DG activation in CoA and pPCx. Moreover, electrophysiological recordings revealed that, in these sites, the level of inhibition was lower than in control animals. These data indicate that early life odor-shock learning produces changes throughout structures of the adult learning circuit that are independent, at least in part, from those involved in infant learning. Moreover, these enduring effects were influenced by the contingency of the infant experience since paired odor-shock produced greater disruption of adult learning and its supporting neural pathway than unpaired presentations. These results suggest that some enduring effects of early life experience are potentiated by contingency and extend beyond brain areas involved in infant learning.
Sevelinges
Yannick
Y
Neurosciences Sensorielles, Comportement, Cognition, CNRS-Université de Lyon, Lyon IFR 19, France. yannicksevelinges@yahoo.fr
Sullivan
Regina M
RM
Messaoudi
Belkacem
B
Mouly
Anne-Marie
AM
D000818:Animals; D000831:Animals, Newborn; D003213:Conditioning, Psychological / Q000502:physiology*; D005071:Evoked Potentials; D005239:Fear / Q000502:physiology* / Q000523:psychology; D007858:Learning / Q000502:physiology*; D008297:Male; D009812:Odorants; D009833:Olfactory Pathways / Q000033:anatomy & histology* / Q000502:physiology*; D051381:Rats; D020318:Rats, Long-Evans
J Neurophysiol. 1988 May;59(5):1352-76
3385464
J Comp Neurol. 1986 Mar 22;245(4):553-65
3009561
J Neurosci. 2004 Jan 21;24(3):652-60
14736851
Eur J Neurosci. 1997 Aug;9(8):1593-602
9283814
J Neurosci. 2005 Oct 5;25(40):9102-11
16207869
Trends Neurosci. 1998 Aug;21(8):323-31
9720596
Brain Res. 2006 May 4;1087(1):142-50
16626646
Dev Psychobiol. 1995 May;28(4):213-9
7621984
J Neurophysiol. 1973 Jul;36(4):775-88
4713319
Proc Natl Acad Sci U S A. 1998 Apr 28;95(9):5335-40
9560276
Horm Behav. 2003 Nov;44(4):338-45
14613728
J Comp Physiol Psychol. 1969 Mar;67(3):370-5
5787388
Physiol Behav. 2001 Jun;73(3):255-60
11438350
Biol Psychiatry. 2000 Dec 15;48(12):1164-74
11137058
J Neuropsychiatry Clin Neurosci. 1997 Summer;9(3):382-402
9276841
Neuroscience. 2001;102(1):11-21
11226666
Eur J Neurosci. 2007 Jun;25(12):3648-58
17610584
Chem Senses. 2001 Jun;26(5):551-76
11418502
Proc Natl Acad Sci U S A. 1996 Feb 20;93(4):1619-23
8643680
Biol Psychiatry. 2007 Nov 15;62(10):1070-9
17826749
Behav Neurosci. 2001 Dec;115(6):1257-72
11770057
J Comp Neurol. 1973 Jul 1;150(1):87-108
4722147
Eur J Neurosci. 2003 Jun;17(11):2457-61
12814377
J Comp Physiol Psychol. 1965 Jun;59:439-42
14313790
Ann N Y Acad Sci. 2004 Dec;1032:63-84
15677396
J Neurosci. 2006 Jun 21;26(25):6737-48
16793881
Behav Neurosci. 1998 Oct;112(5):1092-103
9829787
Neurosci Lett. 1996 Jun 28;211(3):167-70
8817567
J Comp Neurol. 1982 Feb 10;205(1):30-48
7068948
Eur J Neurosci. 2000 Apr;12(4):1516-20
10762380
J Exp Psychol Anim Behav Process. 1978 Apr;4(2):104-19
670888
J Neurophysiol. 1998 Aug;80(2):998-1001
9705487
Ann N Y Acad Sci. 2006 Jul;1071:313-23
16891580
Psychoneuroendocrinology. 2005 Nov;30(10):939-46
15958281
Learn Mem. 2002 Mar-Apr;9(2):66-75
11992017
Physiol Rev. 2003 Jul;83(3):803-34
12843409
J Comp Physiol Psychol. 1962 Aug;55:597-9
14465479
J Comp Neurol. 1978 Mar 15;178(2):255-80
627626
NIDA Res Monogr. 1995;158:172-201
8594484
J Neurophysiol. 1998 Mar;79(3):1425-40
9497422
Int J Dev Neurosci. 1998 Jun-Jul;16(3-4):149-64
9785112
Science. 1979 Aug 31;205(4409):927-9
472715
Neurosci Lett. 1999 Nov 26;276(1):17-20
10586964
Neuroscience. 2006;138(3):901-10
16310958
J Neurophysiol. 2003 Jul;90(1):65-72
12660351
Dev Psychobiol. 1988 Jan;21(1):25-42
3338626
Brain Res. 1986 Apr 23;371(2):400-3
3697770
Annu Rev Physiol. 2002;64:355-405
11826273
J Psychiatry Neurosci. 2007 Jul;32(4):275-84
17653296
Science. 1957 Aug 30;126(3270):405
13467220
Chem Senses. 2000 Oct;25(5):561-73
11015328
Trends Neurosci. 2001 Jul;24(7):381-5
11410267
J Neurosci. 1987 Oct;7(10):3154-62
3668621
Ann N Y Acad Sci. 2003 Apr;985:125-34
12724154
Brain Res. 1986 Jun;392(1-2):278-82
3708381
Nat Rev Neurosci. 2005 Jul;6(7):507-20
15995722
Nature. 2002 May 16;417(6886):282-7
12015602
Proc Natl Acad Sci U S A. 2006 Oct 10;103(41):15206-11
17005727
Chem Senses. 2004 Mar;29(3):225-33
15047597
Dev Psychobiol. 1980 Mar;13(2):141-50
7188912
Neurosci Biobehav Rev. 1999 May;23(5):673-85
10392659
Neuroscience. 2000;98(3):403-6
10869835
Prog Neurobiol. 1998 Jun;55(3):257-332
9643556
J Comp Neurol. 1984 Feb 20;223(2):223-37
6707249
Behav Neurosci. 1991 Apr;105(2):307-12
2043275
Sci Am. 1963 Jun;208:138-46
14026976
Brain Res. 1992 Jul 10;585(1-2):219-28
1511305
Biol Psychiatry. 2005 Apr 15;57(8):823-31
15820702
Learn Mem. 2007 Dec 17;14(12):816-20
18086824
J Neurophysiol. 2000 Jan;83(1):139-45
10634860
J Neurosci Res. 1981;6(1):13-9
7218371
Learn Mem. 2004 Nov-Dec;11(6):761-9
15537739
Behav Brain Res. 2005 Feb 28;157(2):235-44
15639174
Neurosci Biobehav Rev. 2003 Jan-Mar;27(1-2):57-71
12732223
Learn Mem. 2005 Mar-Apr;12(2):120-9
15774945
Science. 1960 Jan 22;131(3395):227-8
13815894
Neuroscience. 2006;137(4):1131-41
16325349
J Comp Neurol. 1983 May 20;216(3):264-91
6306065
Nature. 2000 Sep 7;407(6800):38-9
10993064
Biol Psychol. 2006 Jul;73(1):72-89
16513241
Annu Rev Neurosci. 2000;23:155-84
10845062
Behav Neurosci. 2004 Apr;118(2):274-81
15113251
J Comp Neurol. 2006 Feb 1;494(4):635-50
16374802
Behav Neurosci. 2003 Feb;117(1):184-8
12619920
J Neurosci Methods. 1981 Aug;4(2):189-96
7278369
Science. 1962 Mar 9;135(3506):795-6
14464660
Curr Opin Neurobiol. 1999 Apr;9(2):195-202
10322181