Regulation of fear responses by striatal and extrastriatal adenosine A 2A receptors in forebrain

Biological Psychiatry

Volumn 75, Issue 11, 2014, Pages 855-863

  Wei, Catherine J ^a   Augusto, Elisabete ^a,b,e   Gomes, Catarina A ^b   Singer, Philipp ^c,d   Wang, Yumei ^a   Boison, Detlev ^c   Cunha, Rodrigo A ^b,e   Yee, Benjamin K ^c,d   Chen, Jiang Fan ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c LEGACY RESEARCH   (United States)

^d ETH ZURICH   (Switzerland)

^e UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

anxiety; BDNF; cortex; fear conditioning; hippocampus; startle response; striatum

Indexed keywords

ADENOSINE A2A RECEPTOR; BRAIN DERIVED NEUROTROPHIC FACTOR;

ADENO ASSOCIATED VIRUS; ADULT; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; BEHAVIOR; BRAIN CORTEX; BRAIN REGION; CONDITIONED REFLEX; CONTROLLED STUDY; CORPUS STRIATUM; FEAR; FOREBRAIN; GENOTYPE; HIPPOCAMPUS; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; STARTLE REFLEX; ANIMAL; C57BL MOUSE; GENETICS; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY;

ANIMALS; ANXIETY; CONDITIONING, CLASSICAL; CORPUS STRIATUM; FEAR; HIPPOCAMPUS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PROSENCEPHALON; RECEPTOR, ADENOSINE A2A; REFLEX, STARTLE;

EID: 84900801438     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2013.05.003     Document Type: Article

References (61)

1. S.N. Schiffmann, G. Fisone, R. Moresco, R.A. Cunha, and S. Ferré Adenosine A2A receptors and basal ganglia physiology Prog Neurobiol 83 2007 277 292
2. P. Svenningsson, C. Le Moine, G. Fisone, and B.B. Fredholm Distribution, biochemistry and function of striatal adenosine A2A receptors Prog Neurobiol 59 1999 355 396
3. N. Rebola, R. Lujan, R.A. Cunha, and C. Mulle Adenosine A2A receptors are essential for long-term potentiation of NMDA-EPSCs at hippocampal mossy fiber synapses Neuron 57 2008 121 134
4. Costenla AR, Digenes MJ, Canas PM, Rodrigues RJ, Nogueira C, Maroco J, et al. (2011): Enhanced role of adenosine A(2A) receptors in the modulation of LTP in the rat hippocampus upon ageing. Eur J Neurosci 34:12-21.
5. P. d'Alcantara, C. Ledent, S. Swillens, and S.N. Schiffmann Inactivation of adenosine A2A receptor impairs long term potentiation in the accumbens nucleus without altering basal synaptic transmission Neuroscience 107 2001 455 464
6. M. Flajolet, Z. Wang, M. Futter, W. Shen, N. Nuangchamnong, and J. Bendor et al. FGF acts as a co-transmitter through adenosine A(2A) receptor to regulate synaptic plasticity Nat Neurosci 11 2008 1402 1409
7. A.M. Sebastião, and J.A. Ribeiro Triggering neurotrophic factor actions through adenosine A2A receptor activation: Implications for neuroprotection Br J Pharmacol 158 2009 15 22
8. R.A. Cunha, and P.M. Agostinho Chronic caffeine consumption prevents memory disturbance in different animal models of memory decline J Alzheimers Dis 20 suppl 1 2010 S95 S116
9. R.N. Takahashi, F.A. Pamplona, and R.D. Prediger Adenosine receptor antagonists for cognitive dysfunction: A review of animal studies Front Biosci 13 2008 2614 2632
10. O.P. Dall'igna, P. Fett, M.W. Gomes, D.O. Souza, R.A. Cunha, and D.R. Lara Caffeine and adenosine A(2a) receptor antagonists prevent beta-amyloid (25-35)-induced cognitive deficits in mice Exp Neurol 203 2007 241 245
11. S.R. Kopf, A. Melani, F. Pedata, and G. Pepeu Adenosine and memory storage: Effect of A(1) and A(2) receptor antagonists Psychopharmacology (Berl) 146 1999 214 219
12. G.S. Pereira, J.I. Rossato, J.J. Sarkis, M. Cammarota, C.D. Bonan, and I. Izquierdo Activation of adenosine receptors in the posterior cingulate cortex impairs memory retrieval in the rat Neurobiol Learn Mem 83 2005 217 223
13. M. El Yacoubi, C. Ledent, M. Parmentier, J. Costentin, and J.M. Vaugeois The anxiogenic-like effect of caffeine in two experimental procedures measuring anxiety in the mouse is not shared by selective A(2A) adenosine receptor antagonists Psychopharmacology (Berl) 148 2000 153 163
14. C. Ledent, J.M. Vaugeois, S.N. Schiffmann, T. Pedrazzini, M. El Yacoubi, and J.J. Vanderhaeghen et al. Aggressiveness, hypoalgesia and high blood pressure in mice lacking the adenosine A2a receptor Nature 388 1997 674 678
15. H.Y. Shen, J.E. Coelho, N. Ohtsuka, P.M. Canas, Y.J. Day, and Q.Y. Huang et al. A critical role of the adenosine A2A receptor in extrastriatal neurons in modulating psychomotor activity as revealed by opposite phenotypes of striatum and forebrain A2A receptor knock-outs J Neurosci 28 2008 2970 2975
16. E. Bastia, Y.H. Xu, A.C. Scibelli, Y.J. Day, J. Linden, J.F. Chen, and M.A. Schwarzschild A crucial role for forebrain adenosine A(2A) receptors in amphetamine sensitization Neuropsychopharmacology 30 2005 891 900
17. C.J. Wei, P. Singer, J. Coelho, D. Boison, J. Feldon, B.K. Yee, and J.F. Chen Selective inactivation of adenosine A(2A) receptors in striatal neurons enhances working memory and reversal learning Learn Mem 18 2011 459 474
18. L. Yu, H.Y. Shen, J.E. Coelho, I.M. Araujo, Q.Y. Huang, and Y.J. Day et al. Adenosine A2A receptor antagonists exert motor and neuroprotective effects by distinct cellular mechanisms Ann Neurol 63 2008 338 346
19. T.D. Schmittgen, and K.J. Livak Analyzing real-time PCR data by the comparative C(T) method Nat Protoc 3 2008 1101 1108
20. Hagenbuch N, Feldon J, Yee BK (2006): Use of the elevated plus-maze test with opaque or transparent walls in the detection of mouse strain differences and the anxiolytic effects of diazepam. Behav Pharmacol 17:31-41
21. S. Pietropaolo, M. Mintz, J. Feldon, and B.K. Yee The behavioral sequela following the prevention of home-cage grid-climbing activity in C57BL/6 mice Behav Neurosci 121 2007 345 355
22. B.K. Yee, P. Singer, J.F. Chen, J. Feldon, and D. Boison Transgenic overexpression of adenosine kinase in brain leads to multiple learning impairments and altered sensitivity to psychomimetic drugs Eur J Neurosci 26 2007 3237 3252
23. B.K. Yee, D.L. Chang, and J. Feldon The effects of dizocilpine and phencyclidine on prepulse inhibition of the acoustic startle reflex and on prepulse-elicited reactivity in C57BL6 mice Neuropsychopharmacology 29 2004 1865 1877
24. M.E. Szapacs, T.A. Mathews, L. Tessarollo, W. Ernest Lyons, L.A. Mamounas, and A.M. Andrews Exploring the relationship between serotonin and brain-derived neurotrophic factor: analysis of BDNF protein and extraneuronal 5-HT in mice with reduced serotonin transporter or BDNF expression J Neurosci Methods 140 2004 81 92
25. P. Singer, C.C. Zhang, D. Boison, and B.K. Yee Dysregulation of brain adenosine is detrimental to the expression of conditioned freezing but not general Pavlovian learning Pharmacol Biochem Behav 104 2013 80 89
26. L. Ma, D.D. Wang, T.Y. Zhang, H. Yu, Y. Wang, and S.H. Huang et al. Region-specific involvement of BDNF secretion and synthesis in conditioned taste aversion memory formation J Neurosci 31 2011 2079 2090
27. S.J. Zhou, M.E. Zhu, D. Shu, X.P. Du, X.H. Song, and X.T. Wang et al. Preferential enhancement of working memory in mice lacking adenosine A(2A) receptors Brain Res 1303 2009 74 83
28. N.M. White, and J.A. Salinas Mnemonic functions of dorsal striatum and hippocampus in aversive conditioning Behav Brain Res 142 2003 99 107
29. N.M. White, and M. Viaud Localized intracaudate dopamine D2 receptor activation during the post-training period improves memory for visual or olfactory conditioned emotional responses in rats Behav Neural Biol 55 1991 255 269
30. P.F. Durieux, S.N. Schiffmann, and A. de Kerchove d'Exaerde Differential regulation of motor control and response to dopaminergic drugs by D1R and D2R neurons in distinct dorsal striatum subregions EMBO J 31 2012 640 653
31. M.K. Lobo, H.E. Covington 3rd, D. Chaudhury, A.K. Friedman, H. Sun, and D. Damez-Werno et al. Cell type-specific loss of BDNF signaling mimics optogenetic control of cocaine reward Science 330 2010 385 390
32. H.S. Bateup, E. Santini, W. Shen, S. Birnbaum, E. Valjent, and D.J. Surmeier et al. Distinct subclasses of medium spiny neurons differentially regulate striatal motor behaviors Proc Natl Acad Sci U S A 107 2010 14845 14850
33. T. Hikida, K. Kimura, N. Wada, K. Funabiki, and S. Nakanishi Distinct roles of synaptic transmission in direct and indirect striatal pathways to reward and aversive behavior Neuron 66 2010 896 907
34. J.C. Biedenkapp, and J.W. Rudy Hippocampal and extrahippocampal systems compete for control of contextual fear: Role of ventral subiculum and amygdala Learn Mem 16 2009 38 45
35. S. Bissiére, N. Plachta, D. Hoyer, K.H. McAllister, H.R. Olpe, A.A. Grace, and J.F. Cryan The rostral anterior cingulate cortex modulates the efficiency of amygdala-dependent fear learning Biol Psychiatry 63 2008 821 831
36. B. Sacchetti, E. Baldi, C.A. Lorenzini, and C. Bucherelli Differential contribution of some cortical sites to the formation of memory traces supporting fear conditioning Exp Brain Res 146 2002 223 232
37. S.B. McHugh, M. Fillenz, J.P. Lowry, J.N. Rawlins, and D.M. Bannerman Brain tissue oxygen amperometry in behaving rats demonstrates functional dissociation of dorsal and ventral hippocampus during spatial processing and anxiety Eur J Neurosci 33 2011 322 337
38. A. Adhikari, M.A. Topiwala, and J.A. Gordon Synchronized activity between the ventral hippocampus and the medial prefrontal cortex during anxiety Neuron 65 2010 257 269
39. D.M. Bannerman, J.N. Rawlins, S.B. McHugh, R.M. Deacon, B.K. Yee, and T. Bast et al. Regional dissociations within the hippocampus - memory and anxiety Neurosci Biobehav Rev 28 2004 273 283
40. R.A. Cunha, S. Ferre, J.M. Vaugeois, and J.F. Chen Potential therapeutic interest of adenosine A2A receptors in psychiatric disorders Curr Pharm Des 14 2008 1512 1524
41. S.P. Hamilton, S.L. Slager, A.B. De Leon, G.A. Heiman, D.F. Klein, and S.E. Hodge et al. Evidence for genetic linkage between a polymorphism in the adenosine 2A receptor and panic disorder Neuropsychopharmacology 29 2004 558 565
42. C. Hohoff, E.L. Mullings, S.V. Heatherley, C.M. Freitag, L.C. Neumann, and K. Domschke et al. Adenosine A(2A) receptor gene: Evidence for association of risk variants with panic disorder and anxious personality J Psychiatr Res 44 2010 930 937
43. J. Deckert, M.M. Nöthen, P. Franke, C. Delmo, J. Fritze, and M. Knapp et al. Systematic mutation screening and association study of the A1 and A2a adenosine receptor genes in panic disorder suggest a contribution of the A2a gene to the development of disease Mol Psychiatry 3 1998 81 85
44. D.A. Hince, and M.T. Martin-Iverson Differences in prepulse inhibition (PPI) between Wistar and Sprague-Dawley rats clarified by a new method of PPI standardization Behav Neurosci 119 2005 66 77
45. M.T. Martin-Iverson, and K.N. Stevenson Apomorphine effects on emotional modulation of the startle reflex in rats Psychopharmacology (Berl) 181 2005 60 70
46. C.W. Stoddart, J. Noonan, and M.T. Martin-Iverson Stimulus quality affects expression of the acoustic startle response and prepulse inhibition in mice Behav Neurosci 122 2008 516 526
47. W. Hauber, and M. Koch Adenosine A2a receptors in the nucleus accumbens modulate prepulse inhibition of the startle response Neuroreport 8 1997 1515 1518
48. J. Nagel, H. Schladebach, M. Koch, I. Schwienbacher, C.E. Müller, and W. Hauber Effects of an adenosine A2A receptor blockade in the nucleus accumbens on locomotion, feeding, and prepulse inhibition in rats Synapse 49 2003 279 286
49. M.W. Decker, P. Curzon, and J.D. Brioni Influence of separate and combined septal and amygdala lesions on memory, acoustic startle, anxiety, and locomotor activity in rats Neurobiol Learn Mem 64 1995 156 168
50. M.M. Poo Neurotrophins as synaptic modulators Nat Rev Neurosci 2 2001 24 32
51. M.V. Chao Neurotrophins and their receptors: A convergence point for many signalling pathways Nat Rev Neurosci 4 2003 299 309
52. S.A. Heldt, L. Stanek, J.P. Chhatwal, and K.J. Ressler Hippocampus-specific deletion of BDNF in adult mice impairs spatial memory and extinction of aversive memories Mol Psychiatry 12 2007 656 670
53. O. Bozdagi, E. Rich, S. Tronel, M. Sadahiro, K. Patterson, and M.L. Shapiro et al. The neurotrophin-inducible gene Vgf regulates hippocampal function and behavior through a brain-derived neurotrophic factor-dependent mechanism J Neurosci 28 2008 9857 9869
54. B.K. Yee, S.W. Zhu, A.H. Mohammed, and J. Feldon Levels of neurotrophic factors in the hippocampus and amygdala correlate with anxiety- and fear-related behaviour in C57BL6 mice J Neural Transm 114 2007 431 444
55. Texel SJ, Camandola S, Ladenheim B, Rothman SM, Mughal MR, Unger EL, et al. (2012): Ceruloplasmin deficiency results in an anxiety phenotype involving deficits in hippocampal iron, serotonin, and BDNF. J Neurochem 120:125-134.
56. E. Aso, A. Ozaita, E.M. Valdizán, C. Ledent, A. Pazos, R. Maldonado, and O. Valverde BDNF impairment in the hippocampus is related to enhanced despair behavior in CB1 knockout mice J Neurochem 105 2008 565 572
57. S. Takei, S. Morinobu, S. Yamamoto, M. Fuchikami, T. Matsumoto, and S. Yamawaki Enhanced hippocampal BDNF/TrkB signaling in response to fear conditioning in an animal model of posttraumatic stress disorder J Psychiatr Res 45 2011 460 468
58. N. Kozlovsky, M.A. Matar, Z. Kaplan, M. Kotler, J. Zohar, and H. Cohen Long-term down-regulation of BDNF mRNA in rat hippocampal CA1 subregion correlates with PTSD-like behavioural stress response Int J Neuropsychopharmacol 10 2007 741 758
59. M.T. Tebano, A. Martire, R.L. Potenza, C. Gró, R. Pepponi, and M. Armida et al. Adenosine A(2A) receptors are required for normal BDNF levels and BDNF-induced potentiation of synaptic transmission in the mouse hippocampus J Neurochem 104 2008 279 286
60. F.S. Lee, and M.V. Chao Activation of Trk neurotrophin receptors in the absence of neurotrophins Proc Natl Acad Sci U S A 98 2001 3555 3560
61. N. Assaife-Lopes, V.C. Sousa, D.B. Pereira, J.A. Ribeiro, M.V. Chao, and A.M. Sebastiao Activation of adenosine A2A receptors induces TrkB translocation and increases BDNF-mediated phospho-TrkB localization in lipid rafts: Implications for neuromodulation J Neurosci 30 2010 8468 8480