Increased levels of conditioned fear and avoidance behavior coincide with changes in phosphorylation of the protein kinase B (AKT) within the amygdala in a mouse model of extremes in trait anxiety

Neurobiology of Learning and Memory

Volumn 98, Issue 1, 2012, Pages 56-65

  Yen, Yi Chun ^a   Mauch, Christoph P ^a   Dahlhoff, Maik ^b   Micale, Vincenzo ^a   Bunck, Mirjam ^a   Sartori, Simone B ^c   Singewald, Nicolas ^c   Landgraf, Rainer ^a   Wotjak, Carsten T ^a  

^a MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

Extinction; HAB; Hippocampus; Selective breeding; Spontaneous recovery; Startle

Indexed keywords

PROTEIN KINASE B;

AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY DISORDER; AROUSAL; ARTICLE; AVOIDANCE BEHAVIOR; BASOLATERAL AMYGDALA; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; ENZYME ACTIVITY; FEAR; FEMALE; FREEZING; GENETIC PREDISPOSITION; MALE; MAZE TEST; MOUSE; NONHUMAN; PHOBIA; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; STARTLE REFLEX;

ACOUSTIC STIMULATION; AMYGDALA; ANIMALS; ANXIETY; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; CONDITIONING (PSYCHOLOGY); CUES; DISEASE MODELS, ANIMAL; ELECTROSHOCK; EXTINCTION, PSYCHOLOGICAL; FEAR; MALE; MICE; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT;

EID: 84863091000     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2012.04.009     Document Type: Article

References (68)

1. Barad M. Fear extinction in rodents: Basic insight to clinical promise. Current Opinion in Neurobiology 2005, 15:710-715.
2. Bieszczad K.M., Weinberger N.M. Representational gain in cortical area underlies increase of memory strength. Processing of the National Academy of Sciences, USA 2010, 107:3793-3798.
3. Bouton M.E., Mineka S., Barlow D.H. A modern learning theory perspective on the etiology of panic disorder. Psychology Review 2001, 108:4-32.
4. Bouton M.E., Moody E.W. Memory processes in classical conditioning. Neuroscience and Biobehavioral Reviews 2004, 28:663-674.
5. Bouton M.E., Westbrook R.F., Corcoran K.A., Maren S. Contextual and temporal modulation of extinction: Behavioral and biological mechanisms. Biological Psychiatry 2006, 60:352-360.
6. Charney D.S. Neuroanatomical circuits modulating fear and anxiety behaviors. Acta Psychiatrica Scandinavica, Suppl 2003, 38-50.
7. Dahlhoff M., Siegmund A., Golub Y., Wolf E., Holsboer F., Wotjak C.T. AKT/GSK-3beta/beta-catenin signalling within hippocampus and amygdala reflects genetically determined differences in posttraumatic stress disorder like symptoms. Neuroscience 2010, 169:1216-1226.
8. Davis M. The role of the amygdala in fear and anxiety. Annual Review of Neuroscience 1992, 15:353-375.
9. Davis M., Walker D.L., Miles L., Grillon C. Phasic vs sustained fear in rats and humans: Role of the extended amygdala in fear vs anxiety. Neuropsychopharmacology 2010, 35:105-135.
10. De Boer S.F., Slangen J.L., Van der Gugten J. Plasma catecholamine and corticosterone levels during active and passive shock-prod avoidance behavior in rats: Effects of chlordiazepoxide. Physiology & Behavior 1990, 47:1089-1098.
11. Delgado M.R., Olsson A., Phelps E.A. Extending animal models of fear conditioning to humans. Biological Psychology 2006, 73:39-48.
12. Effting M., Kindt M. Contextual control of human fear associations in a renewal paradigm. Behaviour Research and Therapy 2007, 45:2002-2018.
13. Fanselow M.S. Conditioned and unconditional components of post-shock freezing. Pavlovian Journal of Biological Science 1980, 15:177-182.
14. Fanselow M.S. Associative vs topographical accounts of the immediate shock-freezing deficit in rats: Implications for the response selection rules governing species-specific defensive reactions. Learning and Motivation 1986, 17:16-39.
15. Frankland P.W., Josselyn S.A., Anagnostaras S.G., Kogan J.H., Takahashi E., Silva A.J. Consolidation of CS and US representations in associative fear conditioning. Hippocampus 2004, 14:557-569.
16. Golub Y., Mauch C.P., Dahlhoff M., Wotjak C.T. Consequences of extinction training on associative and non-associative fear in a mouse model of Posttraumatic Stress Disorder (PTSD). Behavioural Brain Research 2009, 205:544-549.
17. Herry C., Ferraguti F., Singewald N., Letzkus J.J., Ehrlich I., Luthi A. Neuronal circuits of fear extinction. European Journal of Neuroscience 2010, 31:599-612.
18. Herry C., Garcia R. Prefrontal cortex long-term potentiation, but not long-term depression, is associated with the maintenance of extinction of learned fear in mice. Journal of Neuroscience 2002, 22:577-583.
19. Herry C., Garcia R. Behavioral and paired-pulse facilitation analyses of long-lasting depression at excitatory synapses in the medial prefrontal cortex in mice. Behavioural Brain Research 2003, 146:89-96.
20. Indovina I., Robbins T.W., Nunez-Elizalde A.O., Dunn B.D., Bishop S.J. Fear-conditioning mechanisms associated with trait vulnerability to anxiety in humans. Neuron 2011, 69:563-571.
21. Irvine E.E., Vernon J., Giese K.P. AlphaCaMKII autophosphorylation contributes to rapid learning but is not necessary for memory. Nature Neuroscience 2005, 8:411-412.
22. Kamprath K., Marsicano G., Tang J., Monory K., Bisogno T., Di Marzo V., et al. Cannabinoid CB1 receptor mediates fear extinction via habituation-like processes. Journal of Neuroscience 2006, 26:6677-6686.
23. Kamprath K., Wotjak C.T. Nonassociative learning processes determine expression and extinction of conditioned fear in mice. Learning & Memory 2004, 11:770-786.
24. Korte S.M., Koolhaas J.M., Wingfield J.C., McEwen B.S. The Darwinian concept of stress: Benefits of allostasis and costs of allostatic load and the trade-offs in health and disease. Neuroscience and Biobehavioral Reviews 2005, 29:3-38.
25. Krishnan V., Han M.H., Graham D.L., Berton O., Renthal W., Russo S.J., et al. Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 2007, 131:391-404.
26. Krömer S.A., Kessler M.S., Milfay D., Birg I.N., Bunck M., Czibere L., et al. Identification of glyoxalase-I as a protein marker in a mouse model of extremes in trait anxiety. Journal of Neuroscience 2005, 25:4375-4384.
27. Landgraf R., Kessler M.S., Bunck M., Murgatroyd C., Spengler D., Zimbelmann M., et al. Candidate genes of anxiety-related behavior in HAB/LAB rats and mice: Focus on vasopressin and glyoxalase-I. Neuroscience and Biobehavioral Reviews 2007, 31:89-102.
28. Landgraf R., Wigger A. High vs low anxiety-related behavior rats: An animal model of extremes in trait anxiety. Behavior Genetics 2002, 32:301-314.
29. Liang K.C., Hon W., Davis M. Pre- and posttraining infusion of N-methyl-D-aspartate receptor antagonists into the amygdala impair memory in an inhibitory avoidance task. Behavioral Neuroscience 1994, 108:241-253.
30. Lin C.H., Yeh S.H., Lu H.Y., Gean P.W. The similarities and diversities of signal pathways leading to consolidation of conditioning and consolidation of extinction of fear memory. Journal of Neuroscience 2003, 23:8310-8317.
31. Lin C.H., Yeh S.H., Lu K.T., Leu T.H., Chang W.C., Gean P.W. A role for the PI-3 kinase signaling pathway in fear conditioning and synaptic plasticity in the amygdala. Neuron 2001, 31:841-851.
32. Lissek S., Powers A.S., McClure E.B., Phelps E.A., Woldehawariat G., Grillon C., et al. Classical fear conditioning in the anxiety disorders: A meta-analysis. Behaviour Research and Therapy 2005, 43:1391-1424.
33. MacLeod C., Rutherford E., Campbell L., Ebsworthy G., Holker L. Selective attention and emotional vulnerability: Assessing the causal basis of their association through the experimental manipulation of attentional bias. Journal of Abnormal Psychology 2002, 111:107-123.
34. Maguschak K.A., Ressler K.J. Beta-catenin is required for memory consolidation. Nature Neuroscience 2008, 11:1319-1326.
35. Manning B.D., Cantley L.C. AKT/PKB signaling: Navigating downstream. Cell 2007, 129:1261-1274.
36. Maren S. Neuroscience. The threatened brain. Science 2007, 317:1043-1044.
37. Marks I., Tobena A. Learning and unlearning fear: A clinical and evolutionary perspective. Neuroscience and Biobehavioral Reviews 1990, 14:365-384.
38. McTeague L.M., Lang P.J., Laplante M.C., Cuthbert B.N., Shumen J.R., Bradley M.M. Aversive imagery in posttraumatic stress disorder: Trauma recurrence, comorbidity, and physiological reactivity. Biological Psychiatry 2010, 67:346-356.
39. Milad M.R., Quirk G.J. Neurons in medial prefrontal cortex signal memory for fear extinction. Nature 2002, 420:70-74.
40. Monfils M.H., Cowansage K.K., Klann E., LeDoux J.E. Extinction-reconsolidation boundaries: Key to persistent attenuation of fear memories. Science 2009, 324:951-955.
41. Mowrer O.H. Basic research methods, statistics and decision theory. American Journal of Occupational Therapy 1960, 14:199-205.
42. Muigg P., Hetzenauer A., Hauer G., Hauschild M., Gaburro S., Frank E., et al. Impaired extinction of learned fear in rats selectively bred for high anxiety-evidence of altered neuronal processing in prefrontal-amygdala pathways. European Journal of Neuroscience 2008, 28:2299-2309.
43. Muigg P., Scheiber S., Salchner P., Bunck M., Landgraf R., Singewald N. Differential stress-induced neuronal activation patterns in mouse lines selectively bred for high, normal or low anxiety. PLoS One 2009, 4:e5346.
44. Myers K.M., Davis M. Behavioral and neural analysis of extinction. Neuron 2002, 36:567-584.
45. North C.S., Suris A.M., Davis M., Smith R.P. Toward validation of the diagnosis of posttraumatic stress disorder. American Journal of Psychiatry 2009, 166:34-41.
46. Pare D., Quirk G.J., Ledoux J.E. New vistas on amygdala networks in conditioned fear. Journal of Neurophysiology 2004, 92:1-9.
47. Paxinos G., Franklin K. The mouse brain in stereotaxic coordinates 2001, Academic Press, San Diego, San Francisco, New York, Boston, London, Sydney, Tokyo.
48. Pitman R.K., Orr S.P., Shalev A.Y., Metzger L.J., Mellman T.A. Psychophysiological alterations in post-traumatic stress disorder. Seminars in Clinical Neuropsychiatry 1999, 4:234-241.
49. Pizzorusso T. Neuroscience. Erasing fear memories. Science 2009, 325:1214-1215.
50. Plendl W., Wotjak C.T. Dissociation of within- and between-session extinction of conditioned fear. Journal of Neuroscience 2010, 30:4990-4998.
51. Ponder C.A., Kliethermes C.L., Drew M.R., Muller J., Das K., Risbrough V.B., et al. Selection for contextual fear conditioning affects anxiety-like behaviors and gene expression. Genes Brain Behav 2007, 6:736-749.
52. Quirk G.J., Mueller D. Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 2008, 33:56-72.
53. Rescorla R.A., Heth C.D. Reinstatement of fear to an extinguished conditioned stimulus. Journal of Experimental Psychology: Animal Behavior Processes 1975, 1:88-96.
54. Ressler K.J., Rothbaum B.O., Tannenbaum L., Anderson P., Graap K., Zimand E., et al. Cognitive enhancers as adjuncts to psychotherapy: Use of D-cycloserine in phobic individuals to facilitate extinction of fear. Archives of General Psychiatry 2004, 61:1136-1144.
55. Riebe C.J., Pamplona F., Kamprath K., Wotjak C.T. Fear relief-toward a new conceptual frame work and what endocannabinoids gotta do with it. Neuroscience 2012, 204:159-185.
56. Robbins S.J. Mechanisms underlying spontaneous recovery in autoshaping. Journal of Experimental Psychology: Animal Behavior Processes 1990, 16:235-249.
57. Rodriguez B.I., Craske M.G., Mineka S., Hladek D. Context-specificity of relapse: Effects of therapist and environmental context on return of fear. Behaviour Research and Therapy 1999, 37:845-862.
58. Rosen J.B., Schulkin J. From normal fear to pathological anxiety. Psychological Review 1998, 105:325-350.
59. Santos J.M., Gargaro A.C., Oliveira A.R., Masson S., Brandao M.L. Pharmacological dissociation of moderate and high contextual fear as assessed by freezing behavior and fear-potentiated startle. European Neuropsychopharmacology 2005, 15:239-246.
60. Sartori S.B., Hauschild M., Bunck M., Gaburro S., Landgraf R., Singewald N. Enhanced fear expression in a psychopathological mouse model of trait anxiety: Pharmacological interventions. PLoS One 2011, 6:e16849.
61. Schiller D., Cain C.K., Curley N.G., Schwartz J.S., Stern S.A., Ledoux J.E., et al. Evidence for recovery of fear following immediate extinction in rats and humans. Learn Mem 2008, 15:394-402.
62. Schiller D., Monfils M.H., Raio C.M., Johnson D.C., Ledoux J.E., Phelps E.A. Preventing the return of fear in humans using reconsolidation update mechanisms. Nature 2010, 463:49-53.
63. Shin L.M., Liberzon I. The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology 2010, 35:169-191.
64. Sullivan G.M., Apergis J., Gorman J.M., LeDoux J.E. Rodent doxapram model of panic: Behavioral effects and c-Fos immunoreactivity in the amygdala. Biological Psychiatry 2003, 53:863-870.
65. Tronson N.C., Corcoran K.A., Jovasevic V., Radulovic J. Fear conditioning and extinction: Emotional states encoded by distinct signaling pathways. Trends in Neurosciences 2012, 35:145-155.
66. Walker D.L., Davis M. Light-enhanced startle: Further pharmacological and behavioral characterization. Psychopharmacology (Berl) 2002, 159:304-310.
67. Westbrook R.F., Iordanova M., McNally G., Richardson R., Harris J.A. Reinstatement of fear to an extinguished conditioned stimulus: Two roles for context. Journal of Experimental Psychology: Animal Behavior Processes 2002, 28:97-110.
68. Yilmazer-Hanke D.M., Wigger A., Linke R., Landgraf R., Schwegler H. Two Wistar rat lines selectively bred for anxiety-related behavior show opposite reactions in elevated plus maze and fear-sensitized acoustic startle tests. Behavior Genetics 2004, 34:309-318.