CREB regulates spine density of lateral amygdala neurons: Implications for memory allocation

Frontiers in Behavioral Neuroscience

Volumn 7, Issue DEC, 2013, Pages

  Sargin, Derya ^a,b   Mercaldo, Valentina ^a,b   Yiu, Adelaide P ^a,b   Higgs, Gemma ^a,b   Han, Jin Hee ^a,b,c   Frankland, Paul W ^a,b   Josselyn, Sheena A ^a,b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

Author keywords

Amygdala; CREB; Dendritic spines; Fear memory; Viral vector

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; VIRUS VECTOR;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CELL STRUCTURE; CONDITIONING; CONTROLLED STUDY; DENDRITIC SPINE; EXPERIMENTAL MOUSE; EXPRESSION VECTOR; FEAR; HUMAN; LATERAL AMYGDALA; MEMORY CONSOLIDATION; MOUSE; NEUROMODULATION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; TRANSCRIPTION REGULATION;

EID: 84891081442     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2013.00209     Document Type: Article

References (65)

1. Aguado, F., Diaz-Ruiz, C., Parlato, R., Martinez, A., Carmona, M. A., Bleckmann, S., et al. (2009). The CREB/CREM transcription factors negatively regulate early synaptogenesis and spontaneous network activity. J. Neurosci. 29, 328-333. doi: 10.1523/JNEUROSCI.5252-08.2009
2. Altarejos, J. Y., and Montminy, M. (2011). CREB and the CRTC co-activators: sensors for hormonal and metabolic signals. Nat. Rev. Mol. Cell Biol. 12, 141-151. doi: 10.1038/nrm3072
3. Bailey, C. H., Bartsch, D., and Kandel, E. R. (1996). Toward a molecular definition of long-term memory storage. Proc. Natl. Acad. Sci. U.S.A. 93, 13445-13452. doi: 10.1073/pnas.93.24.13445
4. Bailey, C. H., and Kandel, E. R. (1993). Structural changes accompanying memory storage. Annu. Rev. Physiol. 55, 397-426. doi: 10.1146/annurev.ph.55.030193.002145
5. Balschun, D., Wolfer, D. P., Gass, P., Mantamadiotis, T., Welzl, H., Schütz, G., et al. (2003). Does cAMP response element-binding protein have a pivotal role in hippocampal synaptic plasticity and hippocampus-dependent memory? J. Neurosci. 23, 6304-6314.
6. Barrot, M., Olivier, J. D. A., Perrotti, L. I., DiLeone, R. J., Berton, O., Eisch, A. J., et al. (2002). CREB activity in the nucleus accumbens shell controls gating of behavioral responses to emotional stimuli. Proc. Natl. Acad. Sci. U.S.A. 99, 11435-11440. doi: 10.1073/pnas.172091899
7. Bartsch, D., Casadio, A., Karl, K. A., Serodio, P., and Kandel, E. R. (1998). CREB1 encodes a nuclear activator, a repressor, and a cytoplasmic modulator that form a regulatory unit critical for long-term facilitation. Cell 95, 211-223. doi: 10.1016/S0092-8674(00)81752-3
8. Bartsch, D., Ghirardi, M., Skehel, P. A., Karl, K. A., Herder, S. P., Chen, M., et al. (1995). Aplysia CREB2 represses long-term facilitation: Relief of repression converts transient facilitation into long-term functional and structural change. Cell 83, 979-992. doi: 10.1016/0092-8674(95)90213-9
9. Bourtchuladze, R., Frenguelli, B., Blendy, J., Cioffi, D., Schütz, G., and Silva, A. J. (1994). Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell 79, 59-68. doi: 10.1016/0092-8674(94)90400-6
10. Cajal, S. R. Y. (1995). Histology of the Nervous System of Man and Vertebrates. New York, NY: Oxford University Press.
11. Campeau, S., and Davis, M. (1995). Involvement of the central nucleus and basolateral complex of the amygdala in fear conditioning measured with fear-potentiated startle in rats trained concurrently with auditory and visual conditioned stimuli. J. Neurosci. 15, 2301-2311.
12. Carlezon, W. A., and Neve, R. L. (2003). Viral-mediated gene transfer to study the behavioral correlates of CREB function in the nucleus accumbens of rats. Methods Mol. Med. 79, 331-350.
13. Cole, C. J., Mercaldo, V., Restivo, L., Yiu, A. P., Sekeres, M. J., Han, J.-H., et al. (2012). MEF2 negatively regulates learning-induced structural plasticity and memory formation. Nat. Neurosci. 15, 1255-1264. doi: 10.1038/ nn.3189
14. Dash, P. K., Hochner, B., and Kandel, E. R. (1990). Injection of the cAMP-responsive element into the nucleus of Aplysia sensory neurons blocks long-term facilitation. Nature 345, 718-721. doi: 10.1038/345718a0
15. Davis, M. (1992). The role of the amygdala in fear and anxiety. Annu. Rev. Neurosci. 15, 353-375. doi: 10.1146/annurev.ne.15.030192.002033
16. Farb, C., Aoki, C., Milner, T., Kaneko, T., and LeDoux, J. (1992). Glutamate immunoreactive terminals in the lateral amygdaloid nucleus: a possible substrate for emotional memory. Brain Res. 593, 145-158. doi: 10.1016/0006-8993(92)91303-V
17. Feldman, M. L., and Dowd, C. (1975). Loss of dendritic spines in aging cerebral cortex. Anat. Embryol. (Berl.) 148, 279-301. doi: 10.1007/BF00319848
18. Gass, P., Wolfer, D. P., Balschun, D., Rudolph, D., Frey, U., Lipp, H. P., et al. (1998). Deficits in memory tasks of mice with CREB mutations depend on gene dosage. Learn. Mem. 5, 274-288.
19. Gruart, A., Benito, E., Delgado-García, J. M., and Barco, A.(2012). Enhanced cAMP response element-binding protein activity increases neuronal excitability, hip-pocampal long-term potentiation, and classical eyeblink conditioning in alert behaving mice. J. Neurosci. 32, 17431-17441. doi: 10.1523/JNEUROSCI.4339-12.2012
20. Guzowski, J. F., and McGaugh, J. L. (1997). Antisense oligodeoxynucleotide-mediated disruption of hippocampal cAMP response element binding protein levels impairs consolidation of memory for water maze training. Proc. Natl. Acad. Sci. U.S.A. 94, 2693-2698. doi: 10.1073/pnas.94. 6.2693
21. Han, J.-H., Kushner, S. A., Yiu, A. P., Cole, C. J., Matynia, A., Brown, R. A., et al. (2007). Neuronal competition and selection during memory formation. Science 316, 457-460. doi: 10.1126/science.1139438
22. Han, J.-H., Kushner, S. A., Yiu, A. P., Hsiang, H.-L., Buch, T., Waisman, A., et al. (2009). Selective erasure of a fear memory. Science 323, 1492-1496. doi: 10.1126/science.1164139
23. Han, J.-H., Yiu, A. P., Cole, C. J., Hsiang, H.-L., Neve, R. L., and Josselyn, S. A. (2008). Increasing CREB in the auditory thalamus enhances memory and generalization of auditory conditioned fear. Learn. Mem. 15, 443-453. doi: 10.1101/lm.993608
24. Harris, K. M., Jensen, F. E., and Tsao, B. (1992). Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation. J. Neurosci. 12, 2685-2705.
25. Harris, K. M., and Stevens, J. K. (1988). Dendritic spines of rat cerebellar Purkinje cells: serial electron microscopy with reference to their biophysical characteristics. J. Neurosci. 8, 4455-4469.
26. Harris, K. M., and Stevens, J. K. (1989). Dendritic spines of CA 1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J. Neurosci. 9, 2982-2997.
27. Harum, K. H., Alemi, L., and Johnston, M. V. (2001). Cognitive impairment in Coffin-Lowry syndrome correlates with reduced RSK2 activation. Neurology 56, 207-214. doi: 10.1212/WNL.56.2.207
28. Horner, C. H., and Arbuthnott, E. (1991). Methods of estimation of spine density- are spines evenly distributed throughout the dendritic field? J. Anat. 177, 179-184.
29. Impey, S., Davare, M., Lesiak, A., Fortin, D., Ando, H., Varlamova, O., et al. (2010). An activity-induced microRNA controls dendritic spine formation by regulating Rac1-PAK signaling. Mol. Cell Neurosci. 43, 146-156. doi: 10.1016/j.mcn.2009.10.005
30. Josselyn, S. A., and Nguyen, P. V. (2005). CREB, synapses and memory disorders: past progress and future challenges. Curr. Drug Targets CNS Neurol. Disord. 4, 481-497. doi: 10.2174/156800705774322058
31. Josselyn, S. A., Shi, C., Carlezon, W. A., Neve, R. L., Nestler, E. J., and Davis, M. (2001). Long-term memory is facilitated by cAMP response element-binding protein overexpression in the amygdala. J. Neurosci. 21, 2404-2412.
32. Kaang, B. K., Kandel, E. R., and Grant, S. G. (1993). Activation of cAMP-responsive genes by stimuli that produce long-term facilitation in Aplysia sensory neurons. Neuron 10, 427-435. doi: 10.1016/0896-6273(93)90331-K
33. Kauffman, A. L., Ashraf, J. M., Corces-Zimmerman, M. R., Landis, J. N., and Murphy, C. T. (2010). Insulin signaling and dietary restriction differentially influence the decline of learning and memory with age. PLoS Biol. 8:e1000372-e1000372. doi: 10.1371/journal.pbio.1000372
34. Kida, S., Josselyn, S. A., Peña de Ortiz, S., Kogan, J. H., Chevere, I., Masushige, S., et al. (2002). CREB required for the stability of new and reactivated fear memories. Nat. Neurosci. 5, 348-355. doi: 10.1038/nn819
35. Lau, H. L., Timbers, T. A., Mahmoud, R., and Rankin, C. H. (2013). Genetic dissection of memory for associative and non-associative learning in Caenorhabditis elegans. Genes Brain Behav.12, 210-223. doi: 10.1111/j.1601-183X.2012. 00863.x
36. LeDoux, J. E., Cicchetti, P., Xagoraris, A., and Romanski, L. M. (1990). The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning. J. Neurosci.10, 1062-1069.
37. Lonze, B. E., Riccio, A., Cohen, S., and Ginty, D. D. (2002). Apoptosis, axonal growth defects, and degeneration of peripheral neurons in mice lacking CREB. Neuron 34, 15-15. doi: 10.1016/S0896-6273(02)00686-4
38. Marie, H., Morishita, W., Yu, X., Calakos, N., and Malenka, R. C. (2005). Generation of silent synapses by acute in vivo expression of CaMKIV and CREB. Neuron 45, 12-12. doi: 10.1016/j.neuron.2005.01.039
39. Matsuzaki, M., Ellis-Davies, G. C., Nemoto, T., Miyashita, Y., Iino, M., and Kasai, H. H. (2001). Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat. Neurosci. 4, 1086-1092. doi: 10.1038/nn736
40. Matsuzaki, M., Honkura, N., Ellis-Davies, G. C. R., and Kasai, H. (2004). Structural basis of long-term potentiation in single dendritic spines. Nature 429, 761-766. doi: 10.1038/nature02617
41. Mayr, B., and Montminy, M. (2001). Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat. Rev. Mol. Cell Biol. 2, 599-609. doi: 10.1038/35085068
42. McDonald, A. J. (1984). Neuronal organization of the lateral and basolat-eral amygdaloid nuclei of the rat. J. Comp. Neurol. 222, 589-606. doi: 10.1002/cne.902220410
43. McDonald, A. J. (1992). "Cell types and intrinsic connections of the amygdala," in The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction, ed J. P. Aggleton (New York, NY: Wiley-Liss), 69-76.
44. Murphy, D. D., and Segal, M. (1997). Morphological plasticity of dendritic spines in central neurons is mediated by activation of cAMP response element binding protein. Proc. Natl. Acad. Sci. U.S.A. 94, 1482-1487. doi: 10.1073/pnas.94.4.1482
45. Pandey, S. C., Roy, A., and Zhang, H. (2003). The decreased phosphorylation of cyclic adenosine monophosphate (cAMP) response element binding (CREB) protein in the central amygdala acts as a molecular substrate for anxiety related to ethanol withdrawal in rats. Alcohol Clin. Exp. Res. 27, 396-409. doi: 10.1097/01.ALC.0000056616.81971.49
46. Pandey, S. C., Zhang, H., Roy, A., and Xu, T. (2005). Deficits in amygdaloid cAMP-responsive element-binding protein signaling play a role in genetic predisposition to anxiety and alcoholism. J. Clin. Invest. 115, 2762-2773. doi: 10.1172/JCI24381
47. Paxinos, G., and Franklin, K. B. J. (2001). The Mouse Brain in Stereotaxic Coordinates. San Diego, Academic Press.
48. Perazzona, B., Isabel, G., Preat, T., and Davis, R. L. (2004). The role of cAMP response element-binding protein in Drosophila long-term memory. J. Neurosci. 24, 8823-8828. doi: 10.1523/JNEUROSCI.4542-03.2004
49. Peters, A., and Kaiserman-Abramof, I. R. (1970). The small pyramidal neuron of the rat cerebral cortex. The perikaryon, dendrites and spines. Dev. Dyn. 127, 321-355.
50. Pittenger, C., Huang, Y. Y., Paletzki, R. F., Bourtchouladze, R., Scanlin, H., Vronskaya, S., et al. (2002). Reversible Inhibition of CREB/ATF Transcription Factors in Region CA1 of the Dorsal Hippocampus Disrupts Hippocampus-Dependent Spatial Memory. Neuron 34, 16-16. doi: 10.1016/S0896-6273(02)00684-0
51. Rexach, J. E., Clark, P. M., Mason, D. E., Neve, R. L., Peters, E. C., and Hsieh-Wilson, L. C. (2012). Dynamic O-GlcNAc modification regulates CREB-mediated gene expression and memory formation. Nat. Chem. Biol. 8, 253-261. doi: 10.1038/nchembio.770
52. Russo, S. J., Wilkinson, M. B., Mazei-Robison, M. S., Dietz, D. M., Maze, I., Krishnan, V., et al. (2009). Nuclear factor kappa B signaling regulates neuronal morphology and cocaine reward. J. Neurosci. 29, 3529-3537. doi: 10.1523/JNEUROSCI.6173-08.2009
53. Sah, P., Faber, E. S., Lopez De Armentia, M., and Power, J. (2003). The amygdaloid complex: anatomy and physiology. Physiol. Rev. 83, 803-834.
54. Silva, A. J., Kogan, J. H., Frankland, P. W., and Kida, S. (1998). CREB and memory. Annu. Rev. Neurosci. 21, 127-148. doi: 10.1146/annurev.neuro.21.1.127
55. Silva, A. J., Simpson, E. M., Takahashi, J. S., Lipp, H-P., Nakanishi, S., Wehner, J. M., et al. (1997). Mutant mice and neuroscience: recommendations concerning genetic background. Neuron 19, 755-759. doi: 10.1016/S0896-6273(00)80958-7
56. Suzuki, S., Zhou, H., Neumaier, J. F., and Pham, T. A. (2007). Opposing functions of CREB and MKK1 synergistically regulate the geometry of dendritic spines in visual cortex. J. Comp. Neurol. 503, 605-617. doi: 10.1002/cne.21424
57. Valverde, O., Mantamadiotis, T., Torrecilla, M., Ugedo, L., Pineda, J., Bleckmann, S., et al. (2004). Modulation of anxiety-like behavior and morphine dependence in CREB-deficient mice. Biol. Psychiatry 29, 1122-1133. doi: 10.1038/sj.npp.1300416
58. Vetere, G., Restivo, L., Cole, C. J., Ross, P. J., Ammassari-Teule, M., Josselyn, S. A., et al. (2011). Spine growth in the anterior cingulate cortex is necessary for the consolidation of contextual fear memory. Proc. Natl. Acad. Sci. U.S.A. 108, 8456-8460. doi: 10.1073/pnas.1016275108
59. Viosca, J., Lopez de Armentia, M., Jancic, D., and Barco, A. (2009). Enhanced CREB-dependent gene expression increases the excitability of neurons in the basal amygdala and primes the consolidation of contextual and cued fear memory. Learn. Mem. 16, 193-197. doi: 10.1101/lm.1254209
60. Wayman, G. A., Impey, S., Marks, D., Saneyoshi, T., Grant, W. F., Derkach, V., et al. (2006). Activity-dependent dendritic arborization mediated by CaM-kinase I activation and enhanced CREB-dependent transcription of Wnt-2. Neuron 50, 897-909. doi: 10.1016/j.neuron.2006.05.008
61. Won, J., and Silva, A. J. (2008). Molecular and cellular mechanisms of memory allocation in neuronetworks. Neurobiol. Learn. Mem. 89, 285-292. doi: 10.1016/j.nlm.2007.08.017
62. Yin, J. C., Del Vecchio, M., Zhou, H., and Tully, T. (1995). CREB as a memory modulator: induced expression of a dCREB2 activator isoform enhances long-term memory in drosophila. Cell 81, 9-9. doi: 10.1016/0092-8674(95) 90375-5
63. Yin, J. C., Wallach, J. S., Del Vecchio, M., Wilder, E. L., Zhou, H., Quinn, W. G., et al. (1994). Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila. Cell 79, 49-58. doi: 10.1016/0092-8674(94)90399-9
64. Yiu, A. P., Rashid, A. J., and Josselyn, S. A. (2011). Increasing CREB function in the CA1 region of dorsal hippocampus rescues the spatial memory deficits in a mouse model of Alzheimer's disease. Neuropsychopharmacology 36, 2169-2186. doi: 10.1038/npp.2011.107
65. Zhou, Y., Won, J., Karlsson, M. G., Zhou, M., Rogerson, T., Balaji, J., et al. (2009). CREB regulates excitability and the allocation of memory to subsets of neurons in the amygdala. Nat. Neurosci.12, 1438-1443. doi: 10.1038/nn.2405