Norepinephrine mediates contextual fear learning and hippocampal pCREB in juvenile rats exposed to predator odor

Neurobiology of Learning and Memory

Volumn 96, Issue 2, 2011, Pages 166-172

  Kabitzke, Patricia A ^a,b   Silva, Lindsay ^c   Wiedenmayer, Christoph ^a,b  

^a NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

Early ontogeny; Fear conditioning; Norepinephrine; PCREB; Predator odor

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; NORADRENALIN; PROPRANOLOL;

AGE DISTRIBUTION; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AVOIDANCE BEHAVIOR; BRAIN LEVEL; BRAIN REGION; CAT; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DORSAL HIPPOCAMPUS; FEAR; FEMALE; HIPPOCAMPUS; JUVENILE ANIMAL; MALE; NEWBORN; NONHUMAN; ODOR CONTROL; OLFACTORY DISCRIMINATION; OLFACTORY MEMORY; PERINATAL PERIOD; PREDATOR AVOIDANCE; PROTEIN PHOSPHORYLATION; RAT; VENTRAL HIPPOCAMPUS;

ADRENERGIC BETA-ANTAGONISTS; ANIMALS; AVOIDANCE LEARNING; CATS; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; FEAR; HIPPOCAMPUS; NOREPINEPHRINE; ODORS; PHOSPHORYLATION; PROPRANOLOL; RATS; RATS, LONG-EVANS;

EID: 79960834395     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2011.04.003     Document Type: Article

References (62)

1. Adamec R., Muir C., Grimes M., Pearcey K. Involvement of noradrenergic and corticoid receptors in the consolidation of the lasting anxiogenic effects of predator stress. Behavioural Brain Research 2007, 179:192-207.
2. Auger A.P., Hexter D.P., McCarthy M.M. Sex difference in the phosphorylation of cAMP response element binding protein (CREB) in neonatal rat brain. Brain Research 2001, 890:110-117.
3. Barnett S.A. An analysis of social behaviour in wild rats. Proceedings of the Zoological Society of London 1958, 130:43.
4. Benarroch E.E. The locus ceruleus norepinephrine system: functional organization and potential clinical significance. Neurology 2009, 73:1699-1704.
5. Bender R.A., Lauterborn J.C., Gall C.M., Cariaga W., Baram T.Z. Enhanced CREB phosphorylation in immature dentate gyrus granule cells precedes neurotrophin expression and indicates a specific role of CREB in granule cell differentiation. European Journal of Neuroscience 2001, 13:679-686.
6. Berridge C.W., Waterhouse B.D. The locus coeruleus-noradrenergic system: Modulation of behavioral state and state-dependent cognitive processes. Brain Research. Brain Research Reviews 2003, 42:33-84.
7. Blanchard R.J., Blanchard D.C. Defensive reactions in the albino rat. Learning and Motivation 1971, 2:351-362.
8. Blanchard R.J., Blanchard D.C. Antipredator defensive behaviors in a visible burrow system. Journal of Comparative Psychology 1989, 103:70-82.
9. Blanchard D.C., Griebel G., Blanchard R.J. Conditioning and residual emotionality effects of predator stimuli: some reflections on stress and emotion. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2003, 27:1177-1185.
10. Blanchard R.J., Yang M., Li C.-I., Gervacio A., Blanchard D.C. Cue and context conditioning of defensive behaviors to cat odor stimuli. Neuroscience & Biobehavioral Reviews 2001, 25:587-595.
11. Bolles R.C., Woods P.J. The ontogeny of behaviour in the albino rat. Animal Behaviour 1964, 12:14.
12. Burman M.A., Gewirtz J.C. Timing of fear expression in trace and delay conditioning measured by fear-potentiated startle in rats. Learning & Memory 2004, 11:205-212.
13. Carlezon W.A., Duman R.S., Nestler E.J. The many faces of CREB. Trends in Neurosciences 2005, 28:436-445.
14. Colussi-Mas J., Panayi F., Scarna H., Renaud B., Berod A., Lambas-Senas L. Blockade of beta-adrenergic receptors prevents amphetamine-induced behavioural sensitization in rats: a putative role of the bed nucleus of the stria terminalis. International Journal of Neuropsychopharmacology 2005, 8:569-581.
15. Daumas S., Halley H., Frances B., Lassalle J.M. Encoding, consolidation, and retrieval of contextual memory: differential involvement of dorsal CA3 and CA1 hippocampal subregions. Learning & Memory 2005, 12:375-382.
16. Davies M.F., Tsui J., Flannery J.A., Li X., DeLorey T.M., Hoffman B.B. Activation of alpha2 adrenergic receptors suppresses fear conditioning: expression of c-Fos and phosphorylated CREB in mouse amygdala. Neuropsychopharmacology 2004, 29:229-239.
17. Debiec J., Ledoux J.E. Disruption of reconsolidation but not consolidation of auditory fear conditioning by noradrenergic blockade in the amygdala. Neuroscience 2004, 129:267-272.
18. Dielenberg R.A., Arnold J.C., McGregor I.S. Low-dose midazolam attenuates predatory odor avoidance in rats. Pharmacology, Biochemistry and Behavior 1999, 62:197-201.
19. Dielenberg R.A., McGregor I.S. Habituation of the hiding response to cat odor in rats (Rattus norvegicus). Journal of Comparative Psychology 1999, 113:376-387.
20. Dielenberg R.A., McGregor I.S. Defensive behavior in rats towards predatory odors: a review. Neuroscience & Biobehavioral Reviews 2001, 25:597-609.
21. Do Monte F.H., Canteras N.S., Fernandes D., Assreuy J., Carobrez A.P. New perspectives on beta-adrenergic mediation of innate and learned fear responses to predator odor. Journal of Neuroscience 2008, 28:13296-13302.
22. Dudai Y. The neurobiology of consolidations, or, how stable is the engram?. Annual Review of Psychology 2004, 55:51-86.
23. Dumas T.C. Late postnatal maturation of excitatory synaptic transmission permits adult-like expression of hippocampal-dependent behaviors. Hippocampus 2005, 15:562-578.
24. Fanselow M.S. Conditional and unconditional components of post-shock freezing. Pavlovian Journal of Biological Sciences 1980, 15:177-181.
25. Grillon C., Cordova J., Morgan C.A., Charney D.S., Davis M. Effects of the beta-blocker propranolol on cued and contextual fear conditioning in humans. Psychopharmacology (Berl) 2004, 175:342-352.
26. Harley C.W., Darby-King A., McCann J., McLean J.H. β1-Adrenoceptor or α1-adrenoceptor activation initiates early odor preference learning in rat pups: Support for the mitral cell/cAMP model of odor preference learning. Learning & Memory 2006, 13:8-13.
27. Hubbard D.T., Blanchard D.C., Yang M., Markham C.M., Gervacio A., Chun-I L., et al. Development of defensive behavior and conditioning to cat odor in the rat. Physiology & Behavior 2004, 80:525-530.
28. Hubbard D.T., Nakashima B.R., Lee I., Takahashi L.K. Activation of basolateral amygdala corticotropin-releasing factor 1 receptors modulates the consolidation of contextual fear. Neuroscience 2007, 150:818-828.
29. Ji J.Z., Wang X.M., Li B.M. Deficit in long-term contextual fear memory induced by blockade of beta-adrenoceptors in hippocampal CA1 region. European Journal of Neuroscience 2003, 17:1947-1952.
30. Joels M., Krugers H., Karst H. Stress-induced changes in hippocampal function. Progress in Brain Research 2007, 167:3-15.
31. Josselyn S.A., Nguyen P.V. CREB, synapses and memory disorders: past progress and future challenges. Current Drug Targets: CNS & Neurological Disorders 2005, 4:481-497.
32. Kogan I., Richter-Levin G. Activation pattern of the limbic system following spatial learning under stress. European Journal of Neuroscience 2008, 27:715-722.
33. LeDoux J.E. Emotion circuits in the brain. Annual Review of Neuroscience 2000, 23:155-184.
34. Lee I., Kesner R.P. Differential contributions of dorsal hippocampal subregions to memory acquisition and retrieval in contextual fear-conditioning. Hippocampus 2004, 14:301-310.
35. McGaugh J.L., Roozendaal B. Role of adrenal stress hormones in forming lasting memories in the brain. Current Opinion in Neurobiology 2002, 12:205-210.
36. McLean J.H., Harley C.W. Olfactory learning in the rat pup: a model that may permit visualization of a mammalian memory trace. NeuroReport 2004, 15:1691-1697.
37. McLean J.H., Harley C.W., Darby-King A., Yuan Q. pCREB in the neonate rat olfactory bulb is selectively and transiently increased by odor preference-conditioned training. Learning & Memory 1999, 6:608-618.
38. Murchison C.F., Zhang X.Y., Zhang W.P., Ouyang M., Lee A., Thomas S.A. A distinct role for norepinephrine in memory retrieval. Cell 2004, 117:131-143.
39. Nowak R.M. Walker's Mammals of the World 1999, The Johns Hopkins University Press, Baltimore. 6th ed.
40. Otto T., Poon P. Dorsal hippocampal contributions to unimodal contextual conditioning. Journal of Neuroscience 2006, 26:6603-6609.
41. Pentkowski N.S., Blanchard D.C., Lever C., Litvin Y., Blanchard R.J. Effects of lesions to the dorsal and ventral hippocampus on defensive behaviors in rats. European Journal of Neuroscience 2006, 23:2185-2196.
42. Pugh C.R., Rudy J.W. A developmental analysis of contextual fear conditioning. Developmental Psychobiology 1996, 29:87-100.
43. Qu L.L., Guo N.N., Li B.M. Beta1- and beta2-adrenoceptors in basolateral nucleus of amygdala and their roles in consolidation of fear memory in rats. Hippocampus 2008, 18:1131-1139.
44. Rodrigues S.M., Schafe G.E., LeDoux J.E. Molecular mechanisms underlying emotional learning and memory in the lateral amygdala. Neuron 2004, 44:75-91.
45. Rudy J.W. Contextual conditioning and auditory cue conditioning dissociate during development. Behavioral Neuroscience 1993, 107:887-891.
46. Rudy J.W., Morledge P. Ontogeny of contextual fear conditioning in rats: implications for consolidation, infantile amnesia, and hippocampal system function. Behavioral Neuroscience 1994, 108:227-234.
47. Sindreu C.B., Scheiner Z.S., Storm D.R. Ca2+ -stimulated adenylyl cyclases regulate ERK-dependent activation of MSK1 during fear conditioning. Neuron 2007, 53:79-89.
48. Sullivan R.M., Landers M., Yeaman B., Wilson D.A. Good memories of bad events in infancy. Nature 2000, 407:38-39.
49. Sullivan R.M., McGaugh J.L., Leon M. Norepinephrine-induced plasticity and one-trial olfactory learning in neonatal rats. Brain Research. Developmental Brain Research 1991, 60:219-228.
50. Sullivan R.M., Stackenwalt G., Nasr F., Lemon C., Wilson D.A. Association of an odor with activation of olfactory bulb noradrenergic beta-receptors or locus coeruleus stimulation is sufficient to produce learned approach responses to that odor in neonatal rats. Behavioral Neuroscience 2000, 114:957-962.
51. Sullivan R.M., Wilson D.A., Leon M. Norepinephrine and learning-induced plasticity in infant rat olfactory system. Journal of Neuroscience 1989, 9:3998-4006.
52. Takahashi L.K., Chan M.M., Pilar M.L. Predator odor fear conditioning: current perspectives and new directions. Neuroscience and Biobehavioral Reviews 2008, 32:1218-1227.
53. Teicher M.H., Barber N.I., Reichheld J.H., Baldessarini R.J., Finklestein S.P. Selective depletion of cerebral norepinephrine with 6-hydroxydopamine and GBR-12909 in neonatal rat. Brain Research 1986, 395:124-128.
54. Thonberg H., Fredriksson J.M., Nedergaard J., Cannon B. A novel pathway for adrenergic stimulation of cAMP-response-element-binding protein (CREB) phosphorylation: mediation via alpha1-adrenoceptors and protein kinase C activation. Biochemical Journal 2002, 364:73-79.
55. Weber M., Watts N., Richardson R. High illumination levels potentiate the acoustic startle response in preweanling rats. Behavioral Neuroscience 2003, 117:1458-1462.
56. Whishaw I.Q., Gharbawie O.A., Clark B.J., Lehmann H. The exploratory behavior of rats in an open environment optimizes security. Behavioural Brain Research 2006, 171:230-239.
57. Wiedenmayer C.P. Adaptations or pathologies? Long-term changes in brain and behavior after a single exposure to severe threat. Neuroscience and Biobehavioral Reviews 2004, 28:1-12.
58. Wiedenmayer C.P., Barr G.A. Ontogeny of defensive behavior and analgesia in rat pups exposed to an adult male rat. Physiology & Behavior 1998, 63:261-269.
59. Wiedenmayer C.P., Magarinos A.M., McEwen B.S., Barr G.A. Age-specific threats induce CRF expression in the paraventricular nucleus of the hypothalamus and hippocampus of young rats. Hormones and Behavior 2005, 47:139-150.
60. Wilson D.A., Best A.R., Sullivan R.M. Plasticity in the olfactory system: lessons for the neurobiology of memory. Neuroscientist 2004, 10:513-524.
61. Wilson D.A., Pham T.C., Sullivan R.M. Norepinephrine and posttraining memory consolidation in neonatal rats. Behavioral Neuroscience 1994, 108:1053-1058.
62. Zhang J.J., Okutani F., Inoue S., Kaba H. Activation of the cyclic AMP response element-binding protein signaling pathway in the olfactory bulb is required for the acquisition of olfactory aversive learning in young rats. Neuroscience 2003, 117:707-713.