A fear-inducing odor alters PER2 and c-Fos expression in brain regions involved in fear memory

PLoS ONE

Volumn 6, Issue 5, 2011, Pages

  Pantazopoulos, Harry ^a,b,c   Dolatshad, Hamid ^a   Davis, Fred C ^a  

^a NORTHEASTERN UNIVERSITY   (United States)

^b MCLEAN HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PER2 PROTEIN; PROTEIN C FOS; 2,4,5 TRIMETHYLTHIAZOLINE; CIRCADIAN RHYTHM SIGNALING PROTEIN; PER2 PROTEIN, MOUSE; THIAZOLE DERIVATIVE;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CENTRAL NUCLEUS (AMYGDALA); CIRCADIAN RHYTHM; CONTROLLED STUDY; FEAR; HIPPOCAMPUS; LIGHT DARK CYCLE; MALE; MEMORY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PYRIFORM CORTEX; SMELLING; SUPRACHIASMATIC NUCLEUS; ANIMAL; BRAIN; C57BL MOUSE; DRUG EFFECT; IMMUNOHISTOCHEMISTRY; METABOLISM; ODOR; PHYSIOLOGY;

ANIMALIA; MUS; RODENTIA;

ANIMALS; BRAIN; FEAR; IMMUNOHISTOCHEMISTRY; MALE; MEMORY; MICE; MICE, INBRED C57BL; ODORS; PERIOD CIRCADIAN PROTEINS; PROTO-ONCOGENE PROTEINS C-FOS; THIAZOLES;

EID: 79957816802     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0020658     Document Type: Article

References (85)

1. Moore RY, (1997) Circadian rhythms: basic neurobiology and clinical applications. Annu Rev Med 48: 253-266.
2. Hastings MH, Herzog ED, (2004) Clock genes, oscillators, and cellular networks in the suprachiasmatic nuclei. J Biol Rhythms 19: 400-413.
3. Reppert SM, Weaver DR, (2002) Coordination of circadian timing in mammals. Nature 418: 935-941.
4. Ko CH, Takahashi JS, (2006) Molecular components of the mammalian circadian clock. Hum Mol Genet 15 Spec No 2: R271-277.
5. Lamia KA, Storch KF, Weitz CJ, (2008) Physiological significance of a peripheral tissue circadian clock. Proc Natl Acad Sci U S A 105: 15172-15177.
6. Storch KF, Lipan O, Leykin I, Viswanathan N, Davis FC, et al. (2002) Extensive and divergent circadian gene expression in liver and heart. Nature 417: 78-83.
7. Schibler U, Ripperger J, Brown SA, (2003) Peripheral circadian oscillators in mammals: time and food. J Biol Rhythms 18: 250-260.
8. Li Z, Ruan L, Lin S, Gittes GK, (2007) Clock controls timing of mouse pancreatic differentiation through regulation of Wnt- and Notch-based and cell division components. Biochem Biophys Res Commun 359: 491-496.
9. Gibbs JE, Beesley S, Plumb J, Singh D, Farrow S, et al. (2009) Circadian timing in the lung; a specific role for bronchiolar epithelial cells. Endocrinology 150: 268-276.
10. Bando H, Nishio T, van der Horst GT, Masubuchi S, Hisa Y, et al. (2007) Vagal regulation of respiratory clocks in mice. J Neurosci 27: 4359-4365.
11. Brown SA, Fleury-Olela F, Nagoshi E, Hauser C, Juge C, et al. (2005) The period length of fibroblast circadian gene expression varies widely among human individuals. PLoS Biol 3: e338.
12. Geyfman M, Andersen B, (2009) How the skin can tell time. J Invest Dermatol 129: 1063-1066.
13. Frigato E, Lunghi L, Ferretti ME, Biondi C, Bertolucci C, (2009) Evidence for circadian rhythms in human trophoblast cell line that persist in hypoxia. Biochem Biophys Res Commun 378: 108-111.
14. Sothern RB, Cornelissen G, Yamamoto T, Takumi T, Halberg F, (2009) Time microscopy of circadian expression of cardiac clock gene mRNA transcription: chronodiagnostic and chrono-therapeutic implications. Clin Ter 160: ep25-34.
15. Leibetseder V, Humpeler S, Svoboda M, Schmid D, Thalhammer T, et al. (2009) Clock genes display rhythmic expression in human hearts. Chronobiol Int 26: 621-636.
16. Vollmers C, Gill S, DiTacchio L, Pulivarthy SR, Le HD, et al. (2009) Time of feeding and the intrinsic circadian clock drive rhythms in hepatic gene expression. Proc Natl Acad Sci U S A 106: 21453-21458.
17. Sherman H, Frumin I, Gutman R, Chapnik N, Lorentz A, et al. Long-term restricted feeding alters circadian expression and reduces the level of inflammatory and disease markers. J Cell Mol Med.
18. Doi R, Oishi K., Ishida N CLOCK regulates circadian rhythms of hepatic glycogen synthesis through transcriptional activation of Gys2. J Biol Chem 285: 22114-22121.
19. Storch KF, Paz C, Signorovitch J, Raviola E, Pawlyk B, et al. (2007) Intrinsic circadian clock of the mammalian retina: importance for retinal processing of visual information. Cell 130: 730-741.
20. Beling I, (1929) Uber das Zeitgedachtnis der Bienen. Zeitschrift fur Vergleichendre Physiologie 9: 259-388.
21. Fuller PM, Lu J, Saper CB, (2008) Differential rescue of light- and food-entrainable circadian rhythms. Science 320: 1074-1077.
22. Carneiro BT, Araujo JF, (2009) The food-entrainable oscillator: a network of interconnected brain structures entrained by humoral signals? Chronobiol Int 26: 1273-1289.
23. Verwey M, Amir S, (2009) Food-entrainable circadian oscillators in the brain. Eur J Neurosci 30: 1650-1657.
24. Mistlberger RE, (2009) Food-anticipatory circadian rhythms: concepts and methods. Eur J Neurosci 30: 1718-1729.
25. Verwey M, Khoja Z, Stewart J, Amir S, (2007) Differential regulation of the expression of Period2 protein in the limbic forebrain and dorsomedial hypothalamus by daily limited access to highly palatable food in food-deprived and free-fed rats. Neuroscience 147: 277-285.
26. O'Brien J, Sutherland RJ, (2007) Evidence for episodic memory in a pavlovian conditioning procedure in rats. Hippocampus 17: 1149-1152.
27. Cain SW, McDonald RJ, Ralph MR, (2008) Time stamp in conditioned place avoidance can be set to different circadian phases. Neurobiol Learn Mem 89: 591-594.
28. Cain SW, Ralph MR, (2009) Circadian modulation of conditioned place avoidance in hamsters does not require the suprachiasmatic nucleus. Neurobiol Learn Mem 91: 81-84.
29. Chaudhury D, Colwell CS, (2002) Circadian modulation of learning and memory in fear-conditioned mice. Behav Brain Res 133: 95-108.
30. Cain SW, Chou T, Ralph MR, (2004) Circadian modulation of performance on an aversion-based place learning task in hamsters. Behav Brain Res 150: 201-205.
31. Loh DH, Navarro J, Hagopian A, Wang LM, Deboer T, Rapid changes in the light/dark cycle disrupt memory of conditioned fear in mice. PLoS One 5.
32. Gerstner JR, Lyons LC, Wright KP Jr, Loh DH, Rawashdeh O, et al. (2009) Cycling behavior and memory formation. J Neurosci 29: 12824-12830.
33. Lamont EW, Robinson B, Stewart J, Amir S, (2005) The central and basolateral nuclei of the amygdala exhibit opposite diurnal rhythms of expression of the clock protein Period2. Proc Natl Acad Sci U S A 102: 4180-4184.
34. Wang LM, Dragich JM, Kudo T, Odom IH, Welsh DK, et al. (2009) Expression of the circadian clock gene Period2 in the hippocampus: possible implications for synaptic plasticity and learned behaviour. ASN Neuro 1.
35. Granados-Fuentes D, Tseng A, Herzog ED, (2006) A circadian clock in the olfactory bulb controls olfactory responsivity. J Neurosci 26: 12219-12225.
36. Gottfried JA Central mechanisms of odour object perception. Nat Rev Neurosci 11: 628-641.
37. LeDoux JE, (2000) Emotion circuits in the brain. Annu Rev Neurosci 23: 155-184.
38. Seidenbecher T, Laxmi TR, Stork O, Pape HC, (2003) Amygdalar and hippocampal theta rhythm synchronization during fear memory retrieval. Science 301: 846-850.
39. Endres T, Fendt M, (2009) Aversion- vs fear-inducing properties of 2,4,5-trimethyl-3-thiazoline, a component of fox odor, in comparison with those of butyric acid. J Exp Biol 212: 2324-2327.
40. Pagani JH, Rosen JB, (2009) The medial hypothalamic defensive circuit and 2,5-dihydro-2,4,5-trimethylthiazoline (TMT) induced fear: comparison of electrolytic and neurotoxic lesions. Brain Res 1286: 133-146.
41. Buron G, Hacquemand R, Pourie G, Lucarz A, Jacquot L, et al. (2007) Comparative behavioral effects between synthetic 2,4,5-trimethylthiazoline (TMT) and the odor of natural fox (Vulpes vulpes) feces in mice. Behav Neurosci 121: 1063-1072.
42. King JA, De Oliveira WL, Patel N, (2005) Deficits in testosterone facilitate enhanced fear response. Psychoneuroendocrinology 30: 333-340.
43. Wallace KJ, Rosen JB, (2000) Predator odor as an unconditioned fear stimulus in rats: elicitation of freezing by trimethylthiazoline, a component of fox feces. Behav Neurosci 114: 912-922.
44. Segall LA, Milet A, Tronche F, Amir S, (2009) Brain glucocorticoid receptors are necessary for the rhythmic expression of the clock protein, PERIOD2, in the central extended amygdala in mice. Neurosci Lett 457: 58-60.
45. Sotres-Bayon F, Cain CK, LeDoux JE, (2006) Brain mechanisms of fear extinction: historical perspectives on the contribution of prefrontal cortex. Biol Psychiatry 60: 329-336.
46. Phelps EA, LeDoux JE, (2005) Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 48: 175-187.
47. Lamont EW, Robinson B, Stewart J, Amir S, (2005) The central and basolateral nuclei of the amygdala exhibit opposite diurnal rhythms of expression of the clock protein Period2. Proceedings of the National Academy of Sciences of the United States of America 102: 4180-4184.
48. Amir S, Stewart J, (2009) Motivational Modulation of Rhythms of the Expression of the Clock Protein PER2 in the Limbic Forebrain. Biological psychiatry 65: 829-834.
49. Kudo T, Loh DH, Kuljis D, Constance C, Colwell CS, (2011) Fast delayed rectifier potassium current: critical for input and output of the circadian system. The Journal of neuroscience: the official journal of the Society for Neuroscience 31: 2746-2755.
50. Hughes AT, Fahey B, Cutler DJ, Coogan AN, Piggins HD, (2004) Aberrant gating of photic input to the suprachiasmatic circadian pacemaker of mice lacking the VPAC2 receptor. J Neurosci 24: 3522-3526.
51. Miller JP, McAuley JD, Pang KC, (2005) Spontaneous fos expression in the suprachiasmatic nucleus of young and old mice. Neurobiology of aging 26: 1107-1115.
52. Sumova A, Travnickova Z, Mikkelsen JD, Illnerova H, (1998) Spontaneous rhythm in c-Fos immunoreactivity in the dorsomedial part of the rat suprachiasmatic nucleus. Brain research 801: 254-258.
53. Li W, Howard JD, Gottfried JA., Disruption of odour quality coding in piriform cortex mediates olfactory deficits in Alzheimer's disease. Brain 133: 2714-2726.
54. Howard JD, Plailly J, Grueschow M, Haynes JD, Gottfried JA, (2009) Odor quality coding and categorization in human posterior piriform cortex. Nat Neurosci 12: 932-938.
55. Suzuki N, Bekkers JM., Distinctive Classes of GABAergic Interneurons Provide Layer-Specific Phasic Inhibition in the Anterior Piriform Cortex. Cereb Cortex.
56. Stettler DD, Axel R, (2009) Representations of odor in the piriform cortex. Neuron 63: 854-864.
57. Funk D, Amir S, (2000) Circadian modulation of fos responses to odor of the red fox, a rodent predator, in the rat olfactory system. Brain Res 866: 262-267.
58. Squire LR, (1992) Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev 99: 195-231.
59. Fortin NJ, Wright SP, Eichenbaum H, (2004) Recollection-like memory retrieval in rats is dependent on the hippocampus. Nature 431: 188-191.
60. Eichenbaum H, (2004) Hippocampus: cognitive processes and neural representations that underlie declarative memory. Neuron 44: 109-120.
61. Chaudhury D, Wang LM, Colwell CS, (2005) Circadian regulation of hippocampal long-term potentiation. J Biol Rhythms 20: 225-236.
62. Doyere V, Debiec J, Monfils MH, Schafe GE, LeDoux JE, (2007) Synapse-specific reconsolidation of distinct fear memories in the lateral amygdala. Nat Neurosci 10: 414-416.
63. Reijmers LG, Perkins BL, Matsuo N, Mayford M, (2007) Localization of a stable neural correlate of associative memory. Science 317: 1230-1233.
64. Gale GD, Anagnostaras SG, Godsil BP, Mitchell S, Nozawa T, et al. (2004) Role of the basolateral amygdala in the storage of fear memories across the adult lifetime of rats. J Neurosci 24: 3810-3815.
65. Debiec J, Doyere V, Nader K, Ledoux JE, (2006) Directly reactivated, but not indirectly reactivated, memories undergo reconsolidation in the amygdala. Proc Natl Acad Sci U S A 103: 3428-3433.
66. Debiec J, Diaz-Mataix L, Bush DE, Doyere V, Ledoux JE., The amygdala encodes specific sensory features of an aversive reinforcer. Nat Neurosci 13: 536-537.
67. Debiec J, Ledoux JE, (2004) Disruption of reconsolidation but not consolidation of auditory fear conditioning by noradrenergic blockade in the amygdala. Neuroscience 129: 267-272.
68. Kajiwara R, Tominaga T, Takashima I, (2007) Olfactory information converges in the amygdaloid cortex via the piriform and entorhinal cortices: observations in the guinea pig isolated whole-brain preparation. Eur J Neurosci 25: 3648-3658.
69. Luskin MB, Price JL, (1983) 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.
70. 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.
71. Pikkarainen M, Ronkko S, Savander V, Insausti R, Pitkanen A, (1999) Projections from the lateral, basal, and accessory basal nuclei of the amygdala to the hippocampal formation in rat. J Comp Neurol 403: 229-260.
72. Pitkanen A, Pikkarainen M, Nurminen N, Ylinen A, (2000) Reciprocal connections between the amygdala and the hippocampal formation, perirhinal cortex, and postrhinal cortex in rat. A review. Ann N Y Acad Sci 911: 369-391.
73. Pitkanen A, Kelly JL, Amaral DG, (2002) Projections from the lateral, basal, and accessory basal nuclei of the amygdala to the entorhinal cortex in the macaque monkey. Hippocampus 12: 186-205.
74. Benes FM, Berretta S, (2000) Amygdalo-entorhinal inputs to the hippocampal formation in relation to schizophrenia. Ann N Y Acad Sci 911: 293-304.
75. Desgranges B, Levy F, Ferreira G, (2008) Anisomycin infusion in amygdala impairs consolidation of odor aversion memory. Brain Res 1236: 166-175.
76. Holahan MR, White NM, (2004) Amygdala c-Fos induction corresponds to unconditioned and conditioned aversive stimuli but not to freezing. Behav Brain Res 152: 109-120.
77. Campeau S, Hayward MD, Hope BT, Rosen JB, Nestler EJ, et al. (1991) Induction of the c-fos proto-oncogene in rat amygdala during unconditioned and conditioned fear. Brain Res 565: 349-352.
78. Segall LA, Perrin JS, Walker CD, Stewart J, Amir S, (2006) Glucocorticoid rhythms control the rhythm of expression of the clock protein, Period2, in oval nucleus of the bed nucleus of the stria terminalis and central nucleus of the amygdala in rats. Neuroscience 140: 753-757.
79. Oster H, Damerow S, Kiessling S, Jakubcakova V, Abraham D, et al. (2006) The circadian rhythm of glucocorticoids is regulated by a gating mechanism residing in the adrenal cortical clock. Cell Metab 4: 163-173.
80. Balsalobre A, Brown SA, Marcacci L, Tronche F, Kellendonk C, et al. (2000) Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science 289: 2344-2347.
81. Roozendaal B, McGaugh JL, (1997) Basolateral amygdala lesions block the memory-enhancing effect of glucocorticoid administration in the dorsal hippocampus of rats. Eur J Neurosci 9: 76-83.
82. McGaugh JL, Cahill L, Roozendaal B, (1996) Involvement of the amygdala in memory storage: interaction with other brain systems. Proc Natl Acad Sci U S A 93: 13508-13514.
83. Thompson BL, Erickson K, Schulkin J, Rosen JB, (2004) Corticosterone facilitates retention of contextually conditioned fear and increases CRH mRNA expression in the amygdala. Behav Brain Res 149: 209-215.
84. Nathan SV, Griffith QK, McReynolds JR, Hahn EL, Roozendaal B, (2004) Basolateral amygdala interacts with other brain regions in regulating glucocorticoid effects on different memory functions. Ann N Y Acad Sci 1032: 179-182.
85. Roozendaal B, McEwen BS, Chattarji S, (2009) Stress, memory and the amygdala. Nat Rev Neurosci 10: 423-433.