BDNF-dependent consolidation of fear memories in the perirhinal cortex

Frontiers in Behavioral Neuroscience

Volumn 7, Issue DEC, 2013, Pages

  Schulz Klaus, Brigitte ^a   Lessmann, Volkmar ^b   Endres, Thomas ^b  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b OTTO VON GUERICKE UNIVERSITY   (Germany)

Author keywords

Brain derived neurotrophic factor; Consolidation; Fear learning; Fear potentiated startle; Perirhinal cortex

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR;

ANALYSIS OF VARIANCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONDITIONING; CONTROLLED STUDY; FEAR; LEARNING; MALE; MEMORY CONSOLIDATION; NONHUMAN; PERIRHINAL CORTEX; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION; STARTLE REFLEX;

EID: 84890891579     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2013.00205     Document Type: Article

References (63)

1. Andero, R., Heldt, S. A., Ye, K., Liu, X., Armario, A., and Ressler, K. J. (2011). Effect of 7,8-Dihydroxyflavone, a small-molecule TrkB agonist, on emotional learning. Am. J. Psychiatry 168, 163-172.doi: 10.1176/appi.ajp.2010.10030326
2. Bang, S. J., and Brown, T. H. (2009). Perirhinal cortex supports acquired fear of auditory objects. Neurobiol. Learn. Mem. 92, 53-62.doi: 10.1016/j.nlm.2009.01. 002
3. Barnes, P., and Thomas, K. L. (2008). Proteolysis of proBDNF is a key regulator in the formation of memory. PLoS One 3:e3248.doi: 10.1371/journal.pone. 0003248
4. Bekinschtein, P., Cammarota, M., Igaz, L. M., Bevilaqua, L. R. M., Izquierdo, I., and Medina, J. H. (2007). Persistence of long-term memory storage requires a late protein synthesis- and BDNF-dependent phase in the hippocampus. Neuron 53, 261-277.doi: 10.1016/j.neuron.2006.11.025
5. Bekinschtein, P., Cammarota, M., Izquierdo, I., and Medina, J. H. (2008). BDNF and memory formation and storage. Neuroscientist 14, 147-156.doi: 10. 1177/1073858407305850
6. Burgos-Robles, A., Vidal-Gonzalez, I., and Quirk, G. J. (2009). Sustained conditioned responses in prelimbic prefrontal neurons are correlated with fear expression and extinction failure. J. Neurosci. 29, 8474-8482.doi: 10.1523/jneurosci. 0378-09.2009
7. Burwell, R. D., Bucci, D. J., Sanborn, M. R., and Jutras, M. J. (2004). Perirhinal and postrhinal contributions to remote memory for context. J. Neurosci. 24, 11023-11028.doi: 10.1523/jneurosci.3781-04.2004
8. Callaghan, C. K., and Kelly, A. M. (2012). Differential BDNF signaling in dentate gyrus and perirhinal cortex during consolidation of recognition memory in the rat. Hippocampus 22, 2127-2135.doi: 10.1002/hipo.22033
9. Campeau, S., and Davis, M. (1995). Involvement of subcortical and cortical afferents to the lateral nucleus of the amygdala in fear conditioning measured with fear-potentiated startle in rats trained concurrently with auditory and visual conditioned stimuli. J. Neurosci. 15, 2312-2327.
10. Choi, D. C., Maguschak, K. A., Ye, K., Jang, S. W., Myers, K. M., and Ressler, K. J. (2010). Prelimbic cortical BDNF is required for memory of learned fear but not extinction or innate fear. Proc. Natl. Acad. Sci. U S A 107, 2675-2680. doi: 10. 1073/pnas.0909359107
11. Cowansage, K.K., Ledoux, J.E., and Monfils, M. H. (2010). Brain-derived neu-rotrophic factor: a dynamic gatekeeper of neural plasticity. Curr. Mol. Pharmacol. 3, 12-29.doi: 10.2174/1874467211003010012
12. Davis, M., Falls, W. A., Campeau, S., and Kim, M. (1993). Fear-potentiated startle: a neural and pharmacological analysis. Behav. Brain Res. 58, 175-198. doi: 10.1016/0166-4328(93)90102-v
13. Endres, T., and Lessmann, V. (2012). Age-dependent deficits in fear learning in heterozygous BDNF knock-out mice. Learn. Mem. 19, 561-570.doi: 10.1101/lm.028068.112
14. Fanselow, M. S., and Gale, G. D. (2003). The amygdala, fear and memory. Ann. N Y Acad. Sci. 985, 125-134.doi: 10.1111/j.1749-6632.2003.tb07077.x
15. Fendt, M., and Fanselow, M. S. (1999). The neuroanatomical and neurochem-ical basis of conditioned fear. Neurosci. Biobehav. Rev. 23, 743-760.doi: 10.1016/s0149-7634(99)00016-0
16. Fendt, M., and Koch, M. (2013). Translational value of startle modulations. Cell Tissue Res. 354, 287-295.doi: 10.1007/s00441-013-1599-5
17. Furtak, S. C., Allen, T. A., and Brown, T. H. (2007). Single-unit firing in rat perirhinal cortex caused by fear conditioning to arbitrary and ecological stimuli. J. Neurosci. 27, 12277-12291.doi: 10.1523/jneurosci.1653-07.2007
18. Gottmann, K., Mittmann, T., and Lessmann, V. (2009). BDNF signaling in the formation, maturation and plasticity of glutamatergic and GABAergic synapses. Exp. Brain Res. 199, 203-234.doi: 10.1007/s00221-009-1994-z
19. Heffner, T. G., Hartman, J. A., and Seiden, L. S. (1980). A rapid method for the regional dissection of the rat brain. Pharmacol. Biochem. Behav. 13, 453-456.doi: 10.1016/0091-3057(80)90254-3
20. Heidbreder, C. A., and Groenewegen, H. J. (2003). The medial prefrontal cortex in the rat: evidence for a dorso-ventral distinction based upon functional and anatomical characteristics. Neurosci. Biobehav. Rev. 27, 555-579. doi: 10.1016/j.neubiorev.2003.09.003
21. Herzog, C., and Otto, T. (1997). Odor-guided fear conditioning in rats: 2. Lesions of the anterior perirhinal cortex disrupt fear conditioned to the explicit conditioned stimulus but not to the training context. Behav. Neurosci. 111, 1265-1272.doi: 10.1037//0735-7044.111.6.1265
22. Herzog, C., and Otto, T. (1998). Contributions of anterior perirhinal cortex to olfactory and contextual fear conditioning. Neuroreport 9, 1855-1859.doi: 10.1097/00001756-199806010-00035
23. Hopkins, M. E., and Bucci, D. J. (2010). BDNF expression in perirhinal cortex is associated with exercise-induced improvement in object recognition memory. Neurobiol. Learn. Mem. 94, 278-284. doi: 10.1016/j.nlm.2010.06.006
24. Hopkins, M. E., Nitecki, R., and Bucci, D. J. (2011). Physical exercise during adolescence versus adulthood: differential effects on object recognition memory and brain-derived neurotrophic factor levels. Neuroscience 194, 84-94.doi: 10.1016/j.neuroscience.2011.07.071
25. Johansen, J. P., Cain, C. K., Ostroff, L. E., and Ledoux, J. E. (2011). Molecular mechanisms of fear learning and memory. Cell 147, 509-524.doi: 10.1016/j.cell.2011.10.009
26. Jones, S. V., Stanek-Rattiner, L., Davis, M., and Ressler, K. J. (2007). Differential regional expression of brain-derived neurotrophic factor following olfactory fear learning. Learn. Mem. 14, 816-820.doi: 10.1101/lm.781507
27. Jovanovic, T., and Ressler, K. J. (2010). How the neurocircuitry and genetics of fear inhibition may inform our understanding of PTSD. Am. J. Psychiatry 167, 648-662.doi: 10.1176/appi.ajp.2009.09071074
28. Kealy, J., and Commins, S. (2011). The rat perirhinal cortex: a review of anatomy, physiology, plasticity and function. Prog. Neurobiol. 93, 522-548.doi: 10.1016/j.pneurobio.2011.03.002
29. Kent, B. A., and Brown, T. H. (2012). Dual functions of perirhinal cortex in fear conditioning. Hippocampus 22, 2068-2079.doi: 10.1002/hipo.22058
30. Kholodar-Smith, D. B., Allen, T. A., and Brown, T. H. (2008). Fear conditioning to discontinuous auditory cues requires perirhinal cortical function. Behav. Neurosci. 122, 1178-1185.doi: 10.1037/a0012902
31. Kloosterman, F., Witter, M. P., and Van, H. T. (2003). Topographical and laminar organization of subicular projections to the parahippocampal region of the rat. J. Comp. Neurol. 455, 156-171.doi: 10.1002/cne. 10472
32. Koenigs, M., and Grafman, J. (2009). Posttraumatic stress disorder: the role of medial prefrontal cortex and amygdala. Neuroscientist 15, 540-548.doi: 10. 1177/1073858409333072
33. Koike, H., Fukumoto, K., Iijima, M., and Chaki, S. (2013). Role of BDNF/TrkB signaling in antidepressant-like effects of a group II metabotropic glutamate receptor antagonist in animal models of depression. Behav. Brain Res. 238, 48-52.doi: 10.1016/j.bbr.2012.10.023
34. LeDoux, J. (2007). The amygdala. Curr. Biol. 17, R868-R874.doi: 10.1016/j.cub. 2007.08.005
35. Li, N., He, X., Zhang, Y., Qi, X., Li, H., Zhu, X., et al. (2011). Brain-derived neurotrophic factor signalling mediates antidepressant effects of lamotrig-ine. Int. J. Neuropsychopharmacol. 14, 1091-1098.doi: 10.1017/s14611457100 01082
36. Lindquist, D. H., Jarrard, L. E., and Brown, T. H. (2004). Perirhinal cortex supports delay fear conditioning to rat ultrasonic social signals. J. Neurosci. 24, 3610-3617.doi: 10.1523/jneurosci.4839-03.2004
37. Mahan, A. L., and Ressler, K. J. (2012). Fear conditioning, synaptic plasticity and the amygdala: implications for posttraumatic stress disorder. Trends Neurosci. 35, 24-35.doi: 10.1016/j.tins.2011.06.007
38. Maren, S. (2001). Neurobiology of Pavlovian fear conditioning. Annu. Rev. Neu-rosci. 24, 897-931.doi: 10.1146/annurev.neuro.24.1.897
39. Matsumoto, T., Rauskolb, S., Polack, M., Klose, J., Kolbeck, R., Korte, M., et al. (2008). Biosynthesis and processing of endogenous BDNF: CNS neurons store and secrete BDNF, not pro-BDNF. Nat. Neurosci. 11, 131-133.doi: 10. 1038/nn2038
40. McIntyre, D. C., Kelly, M. E., and Staines, W. A. (1996). Efferent projections of the anterior perirhinal cortex in the rat. J. Comp. Neurol. 369, 302-318.doi: 10. 1002/(SICI)1096-9861(19960527)369:2<302::AID-CNE10>3.0.CO;2-J
41. Meis, S., Endres, T., and Lessmann, V. (2012). Postsynaptic BDNF signalling regulates long-term potentiation at thalamo-amygdala afferents. J. Physiol. 590, 193-208.doi: 10.1113/jphysiol.2011.220434
42. Munoz, P. C., Aspe, M. A., Contreras, L. S., and Palacios, A. G. (2010). Correlations of recognition memory performance with expression and methylation of brain-derived neurotrophic factor in rats. Biol. Res. 43, 251-258.doi: 10.4067/s0716-97602010000200013
43. Musumeci, G., Sciarretta, C., Rodriguez-Moreno, A., Al, B. M., Negrete-Diaz, V., Costanzi, M., et al. (2009). TrkB modulates fear learning and amygdalar synaptic plasticity by specific docking sites. J. Neurosci. 29, 10131-10143.doi: 10. 1523/JNEUROSCI.1707-09.2009
44. Otto, T., Cousens, G., and Herzog, C. (2000). Behavioral and neuropsychological foundations of olfactory fear conditioning. Behav. Brain Res. 110, 119-128.doi: 10.1016/s0166-4328(99)00190-4
45. Ou, L. C., and Gean, P. W. (2006). Regulation of amygdala-dependent learning by brain-derived neurotrophic factor is mediated by extracellular signal-regulated kinase and phosphatidylinositol-3-kinase. Neuropsychopharmacology 31, 287-296.doi: 10.1038/sj.npp.1300830
46. Ou, L. C., Yeh, S. H., and Gean, P. W. (2010). Late expression of brain-derived neurotrophic factor in the amygdala is required for persistence of fear memory. Neurobiol. Learn. Mem. 93, 372-382.doi: 10.1016/j.nlm.2009.12.003
47. Pang, P. T., Teng, H. K., Zaitsev, E., Woo, N. T., Sakata, K., Zhen, S., et al. (2004). Cleavage of proBDNF by tPA/plasmin is essential for long-term hippocampal plasticity. Science 306, 487-491.doi: 10.1126/science.1100135
48. Pape, H. C., and Pare, D. (2010). Plastic synaptic networks of the amygdala for the acquisition, expression and extinction of conditioned fear. Physiol. Rev. 90, 419-463.doi: 10.1152/physrev.00037.2009
49. Paxinos, G., and Watson, C. (1997). The Rat Brain in Stereotaxic Coordinates. San Diego: Academic Press.
50. Pikkarainen, M., and Pitkanen, A. (2001). Projections from the lateral, basal and accessory basal nuclei of the amygdala to the perirhinal and postrhi-nal cortices in rat. Cereb. Cortex 11, 1064-1082.doi: 10.1093/cercor/11.11. 1064
51. Psotta, L., Lessmann, V., and Endres, T. (2013). Impaired fear extinction learning in adult heterozygous BDNF knock-out mice. Neurobiol. Learn. Mem. 103, 34-38.doi: 10.1016/j.nlm.2013.03.003
52. Rattiner, L. M., Davis, M., French, C. T., and Ressler, K. J. (2004a). Brain-derived neurotrophic factor and tyrosine kinase receptor B involvement in amygdala-dependent fear conditioning. J. Neurosci. 24, 4796-4806.doi: 10.1523/jneurosci. 5654-03.2004
53. Rattiner, L. M., Davis, M., and Ressler, K. J. (2004b). Differential regulation of brain-derived neurotrophic factor transcripts during the consolidation of fear learning. Learn. Mem. 11, 727-731.doi: 10.1101/lm.83304
54. Rattiner, L. M., Davis, M., and Ressler, K. J. (2005). Brain-derived neurotrophic factor in amygdala-dependent learning. Neuroscientist 11, 323-333.doi: 10. 1177/1073858404272255
55. Rogan, M. T., Staubli, U. V., and LeDoux, J. (1997). Fear conditioning induces associative long-term potentiation in the amygdala. Nature 390, 604-607.doi: 10. 1038/37601
56. Sacchetti, B., Lorenzini, C. A., Baldi, E., Tassoni, G., and Bucherelli, C. (1999). Auditory thalamus, dorsal hippocampus, basolateral amygdala and perirhinal cortex role in the consolidation of conditioned freezing to context and to acoustic conditioned stimulus in the rat. J. Neurosci. 19, 9570-9578.
57. Schulz, B., Fendt, M., Richardson, R., and Schnitzler, H. U. (2004). Temporary inactivation of the perirhinal cortex by muscimol injections block acquisition and expression of fear-potentiated startle. Eur. J. Neurosci. 19, 713-720.doi: 10. 1111/j.1460-9568.2004.03180.x
58. Sierra-Mercado, D., Padilla-Coreano, N., and Quirk, G. J. (2011). Dissociable roles of prelimbic and infralimbic cortices, ventral hippocampus and basolateral amygdala in the expression and extinction of conditioned fear. Neuropsy-chopharmacology 36, 529-538.doi: 10.1038/npp.2010.184
59. Sigurdsson, T., Doyere, V., Cain, C. K., and Ledoux, J. E. (2007). Long-term poten-tiation in the amygdala: a cellular mechanism of fear learning and memory. Neuropharmacology 52, 215-227.doi: 10.1016/j.neuropharm.2006.06.022
60. Suzuki, W. A. (1996). The anatomy, physiology and functions of the perirhi-nal cortex. Curr. Opin. Neurobiol. 6, 179-186.doi: 10.1016/s0959-4388(96) 80071-7
61. Suzuki, K., Maekawa, F., Suzuki, S., Nakamori, T., Sugiyama, H., Kanamatsu, T., et al. (2012). Elevated expression of brain-derived neurotrophic factor facilitates visual imprinting in chicks. J. Neurochem. 123, 800-810.doi: 10.1111/jnc.12039
62. Walker, D., Yang, Y., Ratti, E., Corsi, M., Trist, D., and Davis, M. (2009). Differential effects of the CRF-R1 antagonist GSK876008 on fear-potentiated, light- and CRF-enhanced startle suggest preferential involvement in sustained vs phasic threat responses. Neuropsychopharmacology 34, 1533-1542.doi: 10.1038/npp. 2008.210
63. Wetsel, W. C., Rodriguiz, R. M., Guillemot, J., Rousselet, E., Essalmani, R., Kim, I. H., et al. (2013). Disruption of the expression of the proprotein convertase PC7 reduces BDNF production and affects learning and memory in mice. Proc. Natl. Acad. Sci. U S A 110, 17362-17367.doi: 10.1073/pnas.1314698110