Differential dynamics of amino acid release in the amygdala and olfactory cortex during odor fear acquisition as revealed with simultaneous high temporal resolution microdialysis

Learning and Memory

Volumn 16, Issue 11, 2009, Pages 687-697

  Hegoburu, Chloé ^a   Sevelinges, Yannick ^a   Thévenet, Marc ^a   Gervais, Rémi ^a   Parrot, Sandrine ^b   Mouly, Anne Marie ^a  

^a UNIVERSITÉ DE LYON   (France)

^b UNIVERSITÉ LYON 1   (France)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; AMINO ACID; GLUTAMIC ACID;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANTICIPATION; ARTICLE; BRAIN; CONDITIONING; CONTROLLED STUDY; FEAR; FOOTSHOCK; LEARNING; MALE; MEMORY CONSOLIDATION; MICRODIALYSIS; MOLECULAR DYNAMICS; NONHUMAN; ODOR; OLFACTORY CORTEX; PREDICTION; PRIORITY JOURNAL; PYRIFORM CORTEX; RAT; SENSORY STIMULATION; SMELLING; TEMPORAL SUMMATION;

AMINO ACIDS; AMYGDALA; ANALYSIS OF VARIANCE; ANIMALS; CONDITIONING, CLASSICAL; ELECTROSHOCK; FEAR; FREEZING REACTION, CATALEPTIC; MALE; MICRODIALYSIS; NEUROCHEMISTRY; NONLINEAR DYNAMICS; ODORS; OLFACTORY PATHWAYS; RATS; RATS, LONG-EVANS; TIME FACTORS;

EID: 70350675390     PISSN: 10720502     EISSN: 15495485     Source Type: Journal    
DOI: 10.1101/lm.1584209     Document Type: Article

References (84)

1. Armony JL, Quirk GJ, LeDoux JE. 1998. Differential effects of amygdala lesions on early and late plastic components of auditory cortex spike trains during fear conditioning. J Neurosci 18: 2592-2601.
2. Balsam PD, Drew MR, Yang C. 2002. Timing at the start of associative learning. Learn Motiv 33: 141-155.
3. Barnes P, Thomas KL. 2008. Proteolysis of proBDNF is a key regulator in the formation ofmemory. PLoS One 3: e3248. doi: 10.1371/journal.pone.0003248.
4. Bauer EP, Schafe GE, LeDoux JE. 2002. NMDA receptors and L-type voltage-gated calcium channels contribute to long-term potentiation and different components of fear memory formation in the lateral amygdala. J Neurosci 22: 5239-5249.
5. Bechara A, Tranel D, Damasio H, Adolphs R, Rockland C, Damasio AR. 1995. Double- dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. Science 269: 1115-1118.
6. Bert L, Favale D, Jego G, Greve P, Guilloux JP, Guiard BP, Gardier AM, Suaud- Chagny MF, Lestage P. 2004. Rapid and precise method to locate microdialysis probe implantation in the rodent brain. J Neurosci Methods 140: 53-57. (Pubitemid 39625852)
7. Bevins RA, Ayres JJB. 1995. One-trial context fear conditioning as a function of the interstimulus interval. Anim Learn Behav 23: 400-410.
8. Blanchard RJ, Blanchard DC. 1969. Crouching as an index of fear. J Comp Physiol Psychol 67: 370-375.
9. Blanchard RJ, Fukunaga K, Blanchard DC, Kelley MJ. 1975. Conspecific aggression in the laboratory rat. J Comp Physiol Psychol 89: 1204-1209.
10. Buchel C, Morris J, Dolan RJ, Friston KJ. 1998. Brain systems mediating aversive conditioning: An event-related fMRI study. Neuron 20: 947-957. (Pubitemid 28247400)
11. Buhusi CV, Meck WH. 2005. What makes us tick? Functional and neural mechanisms of interval timing. Nat Rev Neurosci 10: 755-765.
12. Cahill L, McGaugh JL. 1998. Mechanisms of emotional arousal and lasting declarative memory. Trends Neurosci 21: 294-299. (Pubitemid 28293639)
13. Chabaud P, Ravel N, Wilson DA, Gervais R. 1999. Functional coupling in rat central olfactory pathways: A coherence analysis. Neurosci Lett 276: 17-20.
14. Chabaud P, Ravel N, Wilson DA, Mouly AM, Vigouroux M, Farget V, Gervais R. 2000. Exposure to behaviourally relevant odour reveals differential characteristics in rat central olfactory pathways as studied through oscillatory activities. Chem Senses 25: 561-573. (Pubitemid 30791966)
15. Collingridge GL, Bliss TV. 1995. Memories of NMDA receptors and LTP. Trends Neurosci 18: 54-56.
16. Cousens G, Otto T. 1998. Both pre- and posttraining excitotoxic lesions of the basolateral amygdala abolish the expression of olfactory and contextual fear conditioning. Behav Neurosci 112: 1092-1103. (Pubitemid 28518992)
17. Datiche F, Cattarelli M. 1996. Reciprocal and topographic connections between the piriform and prefrontal cortices in the rat: A tracing study using the B subunit of the cholera toxin. Brain Res Bull 41: 391-398. (Pubitemid 26427633)
18. Datiche F, Litaudon P, Cattarelli M. 1996. Intrinsic association fiber system of the piriform cortex: A quantitative study based on a cholera toxin B subunit tracing in the rat. J Comp Neurol 376: 265-277. (Pubitemid 26404598)
19. Davis M. 1992. The role of the amygdala in fear and anxiety. Annu Rev Neurosci 15: 353-375.
20. Davis M, Schlesinger LS, Sorenson CA. 1989. Temporal specificity of fear conditioning: Effects of different conditioned stimulus-unconditioned stimulus intervals on the fear-potentiated startle effect. J Exp Psychol Anim Behav Process 15: 295-310.
21. Del Arco A, Mora F. 1999. Effects of endogenous glutamate on extracellular concentrations of GABA, dopamine, and dopamine metabolites in the prefrontal cortex of the freely moving rat: Involvement of NMDA and AMPA/KA receptors. Neurochem Res 24: 1027-1035. (Pubitemid 29406998)
22. Edeline JM, Pham P, Weinberger NM. 1993. Rapid development of learning-induced receptive field plasticity in the auditory cortex. Behav Neurosci 107: 539-551. (Pubitemid 23259620)
23. Ehrlich I, Humeau Y, Grenier F, Ciocchi S, Herry C, Luthi A. 2009. Amygdala inhibitory circuits and the control of fear memory. Neuron 62: 757-771.
24. Goosens KA, Maren S. 2004. NMDA receptors are essential for the acquisition, but not expression, of conditional fear and associative spike firing in the lateral amygdala. Eur J Neurosci 20: 537-548. (Pubitemid 38969639)
25. Haberly LB, Price JL. 1977. The axonal projection patterns of the mitral and tufted cells of the olfactory bulb in the rat. Brain Res 129: 152-157.
26. Haberly LB, Price JL. 1978. Association and commissural fiber systems of the olfactory cortex of the rat. II. Systems originating in the olfactory peduncle. J Comp Neurol 181: 781-807. (Pubitemid 9009545)
27. Jones SV, Stanek-Rattiner L, Davis M, Ressler KJ. 2007. Differential regional expression of brain-derived neurotrophic factor following olfactory fear learning. Learn Mem 14: 816-820.
28. Kadohisa M, Wilson DA. 2006. Separate encoding of identity and similarity of complex familiar odors in piriform cortex. Proc Natl Acad Sci 103: 15206-15211. (Pubitemid 44583189)
29. Kilpatrick L, Cahill L. 2003. Modulation of memory consolidation for olfactory learning by reversible inactivation of the basolateral amygdala. Behav Neurosci 117: 184-188. (Pubitemid 36183889)
30. Kim JJ, Rison RA, Fanselow MS. 1993. Effects of amygdala, hippocampus, and periaqueductal gray lesions on short- and long-term contextual fear. Behav Neurosci 107: 1093-1098.
31. LaBar KS, LeDoux JE, Spencer DD, Phelps EA. 1995. Impaired fear conditioning following unilateral temporal lobectomy in humans. J Neurosci 15: 6846-6855.
32. LaBar KS, Gatenby JC, Gore JC, LeDoux JE, Phelps EA. 1998. Human amygdala activation during conditioned fear acquisition and extinction: A mixed-trial fMRI study. Neuron 20: 937-945.
33. Laurent-Demir C, Jaffard R. 2000. Paradoxical facilitatory effect of fornix lesions on acquisition of contextual fear conditioning in mice. Behav Brain Res 107: 85-91.
34. LeDoux J. 1996. Emotional networks and motor control: A fearful view. Prog Brain Res 107: 437-446. (Pubitemid 26401681)
35. LeDoux JE. 2000. Emotion circuits in the brain. Annu Rev Neurosci 23: 155-184.
36. Lee H, Kim JJ. 1998. Amygdalar NMDA receptors are critical for new fear learning in previously fear-conditioned rats. J Neurosci 18: 8444-8454. (Pubitemid 28465019)
37. Li W, Howard JD, Parrish TB, Gottfried JA. 2008. Aversive learning enhances perceptual and cortical discrimination of indiscriminable odor cues. Science 319: 1842-1845.
38. Litaudon P, Mouly AM, Sullivan R, Gervais R, Cattarelli M. 1997. Learning-induced changes in rat piriform cortex activity mapped using multisite recording with voltage sensitive dye. Eur J Neurosci 9: 1593-1602. (Pubitemid 27348318)
39. Litaudon P, Amat C, Bertrand B, Vigouroux M, Buonviso N. 2003. Piriform cortex functional heterogeneity revealed by cellular responses to odours. Eur J Neurosci 17: 2457-2461. (Pubitemid 36793754)
40. Luskin MB, Price JL. 1983a. The laminar distribution of intracortical fibers originating in the olfactory cortex of the rat. J Comp Neurol 216: 292-302.
41. Luskin MB, Price JL. 1983b. The topographic organization of associational fibers of the olfactory system in the rat, including centrifugal fibers to the olfactory bulb. J Comp Neurol 216: 264-291.
42. Lynch MA. 1989. Mechanisms underlying induction and maintenance of long-term potentiation in the hippocampus. Bioessays 10: 85-90.
43. Majak K, Ronkko S, Kemppainen S, Pitkanen A. 2004. Projections from the amygdaloid complex to the piriform cortex: A PHA-L study in the rat. J Comp Neurol 476: 414-428. (Pubitemid 39025247)
44. Maren S. 2001. Neurobiology of Pavlovian fear conditioning. Annu Rev Neurosci 24: 897-931.
45. Maren S. 2005. Building and burying fear memories in the brain. Neuroscientist 11: 89-99. (Pubitemid 40223093)
46. Maren S, Aharonov G, Fanselow MS. 1996. Retrograde abolition of conditional fear after excitotoxic lesions in the basolateral amygdala of rats: Absence of a temporal gradient. Behav Neurosci 110: 718-726. (Pubitemid 26262447)
47. McClelland JL, McNaughton BL, O'Reilly RC. 1995. Why there are complementary learning systems in the hippocampus and neocortex: Insights from the successes and failures of connectionist models of learning and memory. Psychol Rev 102: 419-457.
48. McDonald AJ. 1998. Cortical pathways to the mammalian amygdala. Prog Neurobiol 55: 257-332.
49. Miserendino MJ, Sananes CB, Melia KR, Davis M. 1990. Blocking of acquisition but not expression of conditioned fear-potentiated startle by NMDA antagonists in the amygdala. Nature 345: 716-718. (Pubitemid 20186547)
50. Mouly AM, Di Scala G. 2006. Entorhinal cortex stimulation modulates amygdala and piriform cortex responses to olfactory bulb inputs in the rat. Neuroscience 137: 1131-1141. (Pubitemid 43133139)
51. Mouly AM, Gervais R. 2002. Polysynaptic potentiation at different levels of rat olfactory pathways following learning. Learn Mem 9: 66-75. (Pubitemid 34507493)
52. Mouly AM, Fort A, Ben-Boutayab N, Gervais R. 2001. Olfactory learning induces differential long-lasting changes in rat central olfactory pathways. Neuroscience 102: 11-21. (Pubitemid 32171850)
53. Ottersen OP. 1982. Connections of the amygdala of the rat. IV: Corticoamygdaloid and intraamygdaloid connections as studied with axonal transport of horseradish peroxidase. J Comp Neurol 205: 30-48.
54. Parrot S, Bert L, Mouly-Badina L, Sauvinet V, Colussi-Mas J, Lambas-Senas L, Robert F, Bouilloux JP, Suaud-Chagny MF, Denoroy L, et al. 2003. Microdialysis monitoring of catecholamines and excitatory amino acids in the rat and mouse brain: Recent developments based on capillary electrophoresis with laser-induced fluorescence detection - a mini-review. Cell Mol Neurobiol 23: 793-804. (Pubitemid 37071501)
55. Parrot S, Sauvinet V, Riban V, Depaulis A, Renaud B, Denoroy L. 2004. High temporal resolution for in vivo monitoring of neurotransmitters in awake epileptic rats using brain microdialysis and capillary electrophoresis with laser-induced fluorescence detection. J Neurosci Methods 140: 29-38. (Pubitemid 39625849)
56. Paxinos G, Watson C. 1998. The rat brain in stereotaxic coordinates, 4th ed. Academic Press, New York.
57. Paz R, Pelletier JG, Bauer EP, Pare D. 2006. Emotional enhancement of memory via amygdala-driven facilitation of rhinal interactions. Nat Neurosci 9: 1321-1329. (Pubitemid 44454274)
58. Price JL. 1973. An autoradiographic study of complementary laminar patterns of termination of afferent fibers to the olfactory cortex. J Comp Neurol 150: 87-108.
59. Quirk GJ, Repa C, LeDoux JE. 1995. Fear conditioning enhances short-latency auditory responses of lateral amygdala neurons: Parallel recordings in the freely behaving rat. Neuron 15: 1029-1039.
60. Quirk GJ, Armony JL, LeDoux JE. 1997. Fear conditioning enhances different temporal components of tone-evoked spike trains in auditory cortex and lateral amygdala. Neuron 19: 613-624.
61. Rodrigues SM, Schafe GE, LeDoux JE. 2001. Intra-amygdala blockade of the NR2B subunit of the NMDA receptor disrupts the acquisition but not the expression of fear conditioning. J Neurosci 21: 6889-6896.
62. Rodrigues SM, Schafe GE, LeDoux JE. 2004. Molecular mechanisms underlying emotional learning and memory in the lateral amygdala. Neuron 44: 75-91.
63. Rosenkranz JA, Grace AA. 2002. Dopamine-mediated modulation of odour-evoked amygdala potentials during Pavlovian conditioning. Nature 417: 282-287.
64. Sah P, Faber ES, Lopez De Armentia M, Power J. 2003. The amygdaloid complex: Anatomy and physiology. Physiol Rev 83: 803-834.
65. Sauvinet V, Parrot S, Benturquia N, Bravo-Moraton E, Renaud B, Denoroy L. 2003. In vivo simultaneous monitoring of γ-aminobutyric acid, glutamate, and L-aspartate using brain microdialysis and capillary electrophoresis with laser-induced fluorescence detection: Analytical developments and in vitro/in vivo validations. Electrophoresis 24: 3187-3196.
66. Savander V, LeDoux JE, Pitkanen A. 1996. Topographic projections from the periamygdaloid cortex to select subregions of the lateral nucleus of the amygdala in the rat. Neurosci Lett 211: 167-170. (Pubitemid 26290886)
67. Sevelinges Y, Gervais R, Messaoudi B, Granjon L, Mouly AM. 2004. Olfactory fear conditioning induces field potential potentiation in rat olfactory cortex and amygdala. Learn Mem 11: 761-769. (Pubitemid 39602517)
68. Sevelinges Y, Moriceau S, Holman P, Miner C, Muzny K, Gervais R, Mouly AM, Sullivan RM. 2007. Enduring effects of infant memories: Infant odor-shock conditioning attenuates amygdala activity and adult fear conditioning. Biol Psychiatry 62: 1070-1079. (Pubitemid 350047460)
69. Sevelinges Y, Sullivan RM, Messaoudi B, Mouly AM. 2008. Neonatal odor-shock conditioning alters the neural network involved in odor fear learning at adulthood. Learn Mem 15: 649-656.
70. Stork O, Ji FY, Obata K. 2002. Reduction of extracellular GABA in the mouse amygdala during and following confrontation with a conditioned fear stimulus. Neurosci Lett 327: 138-142. (Pubitemid 34722426)
71. Suzuki N, Bekkers JM. 2007. Inhibitory interneurons in the piriform cortex. Clin Exp Pharmacol Physiol 34: 1064-1069.
72. Venton BJ, Robinson TE, Kennedy RT, Maren S. 2006. Dynamic amino acid increases in the basolateral amygdala during acquisition and expression of conditioned fear. Eur J Neurosci 23: 3391-3398. (Pubitemid 43911718)
73. Walker DL, Davis M. 1997. Double dissociation between the involvement of the bed nucleus of the stria terminalis and the central nucleus of the amygdala in startle increases produced by conditioned versus unconditioned fear. J Neurosci 17: 9375-9383. (Pubitemid 27498464)
74. Walker DL, Davis M. 2002. The role of amygdala glutamate receptors in fear learning, fear-potentiated startle, and extinction. Pharmacol Biochem Behav 71: 379-392. (Pubitemid 34117707)
75. Walker DL, Paschall GY, Davis M. 2005. Glutamate receptor antagonist infusions into the basolateral and medial amygdala reveal differential contributions to olfactory vs. context fear conditioning and expression. Learn Mem 12: 120-129. (Pubitemid 40517078)
76. Watson CJ, Venton BJ, Kennedy RT. 2006. In vivo measurements of neurotransmitters by microdialysis sampling. Anal Chem78: 1391-1399.
77. Weinberger NM. 2004. Specific long-term memory traces in primary auditory cortex. Nat Rev Neurosci 5: 279-290.
78. Weinberger NM, Bakin JS. 1998. Learning-induced physiological memory in adult primary auditory cortex: Receptive fields plasticity, model, and mechanisms. Audiol Neurootol 3: 145-167.
79. Weinberger NM, Javid R, Lepan B. 1995. Heterosynaptic long-term facilitation of sensory-evoked responses in the auditory cortex by stimulation of the magnocellular medial geniculate body in guinea pigs. Behav Neurosci 109: 10-17.
80. Wilson DA. 1998a. Habituation of odor responses in the rat anterior piriform cortex. J Neurophysiol 79: 1425-1440. (Pubitemid 28125376)
81. Wilson DA. 1998b. Synaptic correlates of odor habituation in the rat anterior piriform cortex. J Neurophysiol 80: 998-1001. (Pubitemid 28387678)
82. Wilson DA. 2000. Odor specificity of habituation in the rat anterior piriform cortex. J Neurophysiol 83: 139-145.
83. Wilson DA, Stevenson RJ. 2003. Olfactory perceptual learning: The critical role of memory in odor discrimination. Neurosci Biobehav Rev 27: 307-328.
84. Young AM. 2004. Increased extracellular dopamine in nucleus accumbens in response to unconditioned and conditioned aversive stimuli: Studies using 1 min microdialysis in rats. J Neurosci Methods 138: 57-63.