CREB regulates excitability and the allocation of memory to subsets of neurons in the amygdala

Nature Neuroscience

Volumn 12, Issue 11, 2009, Pages 1438-1443

  Zhou, Yu ^a,b,c,f   Won, Jaejoon ^a,b,c   Karlsson, Mikael Guzman ^a,b,c   Zhou, Miou ^a,b,c   Rogerson, Thomas ^a,b,c   Balaji, Jayaprakash ^a,b,c   Neve, Rachael ^d   Poirazi, Panayiota ^e   Silva, Alcino J ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^e INSTITUTE OF MOLECULAR BIOLOGY AND BIOTECHNOLOGY   (Greece)

^f QINGDAO UNIVERSITY MEDICAL COLLEGE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALLATOSTATIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; G PROTEIN COUPLED RECEPTOR; HERPESVIRUS VECTOR; ALSTR PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; GREEN FLUORESCENT PROTEIN; HORMONE ANTAGONIST; NEUROPEPTIDE; NEUROPEPTIDE RECEPTOR;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL SUBPOPULATION; CONDITIONING; CONTROLLED STUDY; DROSOPHILA; FEAR; FLUORESCENCE; MEMORY; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; ANALYSIS OF VARIANCE; ANIMAL; AUDITORY STIMULATION; BIOPHYSICS; C57BL MOUSE; CYTOLOGY; DRUG EFFECT; ELECTROSTIMULATION; GENE TRANSFER; GENETICS; IN VITRO STUDY; METABOLISM; METHODOLOGY; PATCH CLAMP; PHYSIOLOGY; SIMPLEXVIRUS;

ACOUSTIC STIMULATION; AMYGDALA; ANALYSIS OF VARIANCE; ANIMALS; BIOPHYSICS; CONDITIONING (PSYCHOLOGY); CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DROSOPHILA; DROSOPHILA PROTEINS; ELECTRIC STIMULATION; FEAR; GENE TRANSFER TECHNIQUES; GREEN FLUORESCENT PROTEINS; HORMONE ANTAGONISTS; MEMORY; MICE; MICE, INBRED C57BL; NEURONS; NEUROPEPTIDES; PATCH-CLAMP TECHNIQUES; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, NEUROPEPTIDE; SIMPLEXVIRUS;

EID: 74949102638     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.2405     Document Type: Article

References (44)

1. Repa, J.C. et al. Two different lateral amygdala cell populations contribute to the initiation and storage of memory. Nat. Neurosci. 4, 724-731 (2001). (Pubitemid 32595411)
2. Rumpel, S., LeDoux, J., Zador, A. & Malinow, R. Postsynaptic receptor trafficking underlying a form of associative learning. Science 308, 83-88 (2005). (Pubitemid 40471002)
3. Reijmers, L.G., Perkins, B.L., Matsuo, N. & Mayford, M. Localization of a stable neural correlate of associative memory. Science 317, 1230-1233 (2007).
4. Schafe, G.E., Doyere, V. & LeDoux, J.E. Tracking the fear engram: the lateral amygdala is an essential locus of fear memory storage. J. Neurosci. 25, 10010-10014 (2005).
5. Han, J.H. et al. Neuronal competition and selection during memory formation. Science 316, 457-460 (2007).
6. Han, J.H. et al. Selective erasure of a fear memory. Science 323, 1492-1496 (2009).
7. Clark, M.S. et al. Overexpression of 5-HT1B receptor in dorsal raphe nucleus using herpes simplex virus gene transfer increases anxiety behavior after inescapable stress. J. Neurosci. 22, 4550-4562 (2002). (Pubitemid 37465671)
8. Birgül, N., Weise, C., Kreienkamp, H.J. & Richter, D. Reverse physiology in Drosophila: identification of a novel allatostatin-like neuropeptide and its cognate receptor structurally related to the mammalian somatostatin/galanin/opioid receptor family. EMBO J. 18, 5892-5900 (1999). (Pubitemid 29515666)
9. Karschin, C., Dissmann, E., Stuhmer, W. & Karschin, A. IRK(1-3) and GIRK(1-4) inwardly rectifying K+ channel mRNAs are differentially expressed in the adult rat brain. J. Neurosci. 16, 3559-3570 (1996). (Pubitemid 26149495)
10. Tan, E.M. et al. Selective and quickly reversible inactivation of mammalian neurons in vivo using the Drosophila allatostatin receptor. Neuron 51, 157-170 (2006). (Pubitemid 44041867)
11. Tan, W. et al. Silencing preBotzinger complex somatostatin-expressing neurons induces persistent apnea in awake rat. Nat. Neurosci. 11, 538-540 (2008). (Pubitemid 351595198)
12. Lechner, H.A., Lein, E.S. & Callaway, E.M. A genetic method for selective and quickly reversible silencing of mammalian neurons. J. Neurosci. 22, 5287-5290 (2002). (Pubitemid 35386449)
13. Kida, S. et al. CREB required for the stability of new and reactivated fear memories. Nat. Neurosci. 5, 348-355 (2002). (Pubitemid 34279815)
14. Bourtchuladze, R. et al. Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element binding protein. Cell 79, 59-68 (1994).
15. Yamamoto, T., Shimura, T., Sako, N., Yasoshima, Y. & Sakai, N. Neural substrates for conditioned taste aversion in the rat. Behav. Brain Res. 65, 123-137 (1994).
16. Lamprecht, R., Hazvi, S. & Dudai, Y. cAMP response element binding protein in the amygdala is required for long- but not short-term conditioned taste aversion memory. J. Neurosci. 17, 8443-8450 (1997). (Pubitemid 27461065)
17. Josselyn, S.A., Kida, S. & Silva, A.J. Inducible repression of CREB function disrupts amygdala-dependent memory. Neurobiol. Learn. Mem. 82, 159-163 (2004). (Pubitemid 39070261)
18. McKernan, M.G. & Shinnick-Gallagher, P. Fear conditioning induces a lasting potentiation of synaptic currents in vitro. Nature 390, 607-611 (1997). (Pubitemid 28016194)
19. Huang, Y.Y. & Kandel, E.R. Postsynaptic induction and PKA-dependent expression of LTP in the lateral amygdala. Neuron 21, 169-178 (1998). (Pubitemid 28355701)
20. Han, M.H. et al. Role of cAMP response element-binding protein in the rat locus ceruleus: regulation of neuronal activity and opiate withdrawal behaviors. J. Neurosci. 26, 4624-4629 (2006).
21. Dong, Y. et al. CREB modulates excitability of nucleus accumbens neurons. Nat. Neurosci. 9, 475-477 (2006).
22. Viosca, J., Lopez de Armentia, M., Jancic, D. & Barco, A. 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 (2009).
23. Murphy, G.G. et al. Increased neuronal excitability, synaptic plasticity, and learning in aged Kvbeta1.1 knockout mice. Curr. Biol. 14, 1907-1915 (2004). (Pubitemid 39464813)
24. Faber, E.S., Callister, R.J. & Sah, P. Morphological and electrophysiological properties of principal neurons in the rat lateral amygdala in vitro. J. Neurophysiol. 85, 714-723 (2001). (Pubitemid 32147773)
25. Storm, J.F. Potassium currents in hippocampal pyramidal cells. Prog. Brain Res. 83, 161-187 (1990). (Pubitemid 20205278)
26. Oh, M.M., McKay, B.M., Power, J.M. & Disterhoft, J.F. Learning-related postburst afterhyperpolarization reduction in CA1 pyramidal neurons is mediated by protein kinase A. Proc. Natl. Acad. Sci. USA 106, 1620-1625 (2009).
27. Santini, E., Quirk, G.J. & Porter, J.T. Fear conditioning and extinction differentially modify the intrinsic excitability of infralimbic neurons. J. Neurosci. 28, 4028-4036 (2008).
28. Staff, N.P. & Spruston, N. Intracellular correlate of EPSP-spike potentiation in CA1 pyramidal neurons is controlled by GABAergic modulation. Hippocampus 13, 801-805 (2003). (Pubitemid 37407966)
29. Carvalho, T.P. & Buonomano, D.V. Differential effects of excitatory and inhibitory plasticity on synaptically driven neuronal input-output functions. Neuron 61, 774-785 (2009).
30. Losonczy, A., Makara, J.K. & Magee, J.C. Compartmentalized dendritic plasticity and input feature storage in neurons. Nature 452, 436-441 (2008). (Pubitemid 351450839)
31. Silva, A.J., Kogan, J.H., Frankland, P.W. & Kida, S. CREB and memory. Annu. Rev. Neurosci. 21, 127-148 (1998). (Pubitemid 28150661)
32. Shaywitz, A.J. & Greenberg, M.E. CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu. Rev. Biochem. 68, 821-861 (1999). (Pubitemid 29449210)
33. Mayr, B. & Montminy, M. Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat. Rev. Mol. Cell Biol. 2, 599-609 (2001). (Pubitemid 33674011)
34. Lonze, B.E. & Ginty, D.D. Function and regulation of CREB family transcription factors in the nervous system. Neuron 35, 605-623 (2002). (Pubitemid 35229980)
35. Carlezon, W.A. Jr., Duman, R.S. & Nestler, E.J. The many faces of CREB. Trends Neurosci. 28, 436-445 (2005). (Pubitemid 40982557)
36. Jancic, D., Lopez de Armentia, M., Valor, L.M., Olivares, R. & Barco, A. Inhibition of cAMP response element binding protein reduces neuronal excitability and plasticity, and triggers neurodegeneration. Cereb. Cortex published online, doi:10.1093/cercor/bhp004 (12 February 2009).
37. Won, J. & Silva, A.J. Molecular and cellular mechanisms of memory allocation in neuronetworks. Neurobiol. Learn. Mem. 89, 285-292 (2008). (Pubitemid 351318270)
38. Sassone-Corsi, P. Transcription factors responsive to cAMP. Annu. Rev. Cell Dev. Biol. 11, 355-377 (1995). (Pubitemid 26019608)
39. Lim, F. & Neve, R.L. Current Protocols in Neuroscience (Greene Publishing Assoc. and Wiley-Interscience, New York, 1999).
40. Paxinos, G. & Franklin, K.B.J. The Mouse Brain in Stereotaxic Coordinates (Academic Press, San Diego, 2003).
41. Barrot, M. et al. CREB activity in the nucleus accumbens shell controls gating of behavioral responses to emotional stimuli. Proc. Natl. Acad. Sci. USA 99, 11435-11440 (2002). (Pubitemid 34920943)
42. Faber, E.S. & Sah, P. Opioids inhibit lateral amygdala pyramidal neurons by enhancing a dendritic potassium current. J. Neurosci. 24, 3031-3039 (2004). (Pubitemid 38405750)
43. Liebmann, L. et al. Differential effects of corticosterone on the slow afterhyperpolarization in the basolateral amygdala and CA1 region: possible role of calcium channel subunits. J. Neurophysiol. 99, 958-968 (2008). (Pubitemid 351253248)
44. Humeau, Y. et al. A pathway-specific function for different AMPA receptor subunits in amygdala long-term potentiation and fear conditioning. J. Neurosci. 27, 10947-10956 (2007). (Pubitemid 47574151)