Fear extinction induces mGluR5-mediated synaptic and intrinsic plasticity in infralimbic neurons

Journal of Neuroscience

Volumn 33, Issue 17, 2013, Pages 7184-7193

  Sepulveda Orengo, Marian T ^a   Lopez, Ana V ^a   Soler Cedeño, Omar ^a   Porter, James T ^a  

^a PONCE SCHOOL OF MEDICINE   (Puerto Rico)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; METABOTROPIC RECEPTOR 5; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; CONDITIONING; CONTROLLED STUDY; EVOKED RESPONSE; EXCITATORY POSTSYNAPTIC POTENTIAL; FEAR; INHIBITORY POSTSYNAPTIC POTENTIAL; MALE; NERVE CELL PLASTICITY; NERVE EXCITABILITY; NERVE POTENTIAL; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; TRAINING; VIDEO MICROSCOPY;

ANIMALS; EXCITATORY AMINO ACID ANTAGONISTS; EXTINCTION, PSYCHOLOGICAL; FEAR; LIMBIC SYSTEM; MALE; NEURONAL PLASTICITY; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, METABOTROPIC GLUTAMATE; SYNAPSES;

EID: 84876552528     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5198-12.2013     Document Type: Article

References (68)

1. Abel HJ, Lee JC, Callaway JC, Foehring RC (2004) Relationships between intracellular calcium and afterhyperpolarizations in neocortical pyramidal neurons. J Neurophysiol 91:324-335. Medline
2. Amano T, Unal CT, Paré D (2010) Synaptic correlates of fear extinction in the amygdala. Nat Neurosci 13:489-494. CrossRef Medline
3. Ayala JE, Chen Y, Banko JL, Sheffler DJ, Williams R, Telk AN, Watson NL, Xiang Z, Zhang Y, Jones PJ, Lindsley CW, Olive MF, Conn PJ (2009) mGluR5 positive allosteric modulators facilitate both hippocampal ltp and ltd and enhance spatial learning. Neuropsychopharmacology 34: 2057-2071. CrossRef Medline
4. Benito E, Barco A (2010) CREB's control of intrinsic and synaptic plasticity: implications for CREB-dependent memory models. Trends Neurosci 33: 230-240. CrossRef Medline
5. Blanchard DC, Blanchard RJ (1972) Innate and conditioned reactions to threat in rats with amygdaloid lesions. J Comp Physiol Psychol 81:281-290. CrossRef Medline
6. Boehm J, Kang MG, Johnson RC, Esteban J, Huganir RL, Malinow R (2006) Synaptic incorporation of AMPA receptors during LTP is controlled by a PKC phosphorylation site on GluR1. Neuron 51:213-225. CrossRef Medline
7. Burgos-Robles A, Vidal-Gonzalez I, Santini E, Quirk GJ (2007) Consolidation of Fear Extinction RequiresNMDAReceptor-Dependent Bursting in the Ventromedial Prefrontal Cortex. Neuron 53:871-880. CrossRef Medline
8. Cabezas C, Buno W (2006) Distinct transmitter release properties determine differences in short-term plasticity at functional and silent synapses. J Neurophysiol 95:3024-3034. CrossRef Medline
9. Clem RL, Barth A (2006) Pathway-specific trafficking of native AMPARs by in vivo experience. Neuron 49:663-670. CrossRef Medline
10. Clem RL, Huganir RL (2010) Calcium-permeable AMPA receptor dynamics mediate fear memory erasure. Science 330:1108-1112. CrossRef Medline
11. Clem RL, Celikel T, Barth AL (2008) Ongoing in vivo experience triggers synaptic metaplasticity in the neocortex. Science 319:101-104. CrossRef Medline
12. Clem RL, Anggono V, Huganir RL (2010) PICK1 regulates incorporation of calcium-permeable AMPA receptors during cortical synaptic strengthening. J Neurosci 30:6360-6366. CrossRef Medline
13. Cull-Candy S, Kelly L, Farrant M (2006) Regulation of Ca2+-permeable AMPA receptors: synaptic plasticity and beyond. Curr Opin Neurobiol 16:277-280. CrossRef Medline
14. Duvarci S, Paré D (2007) Glucocorticoids enhance the excitability of principal basolateral amygdala neurons. J Neurosci 27:4482-4491. CrossRef Medline
15. Ehrlich I, Humeau Y, Grenier F, Ciocchi S, Herry C, Luthi A (2009) Amygdala inhibitory circuits and the control of fear memory. Neuron 62:757-771. CrossRef Medline
16. El-Hassar L, Hagenston AM, D'Angelo LB, Yeckel MF (2011) Metabotropic glutamate receptors regulate hippocampal CA1 pyramidal neuron excitability via Ca(2)(+) wave-dependent activation of SK and TRPC channels. J Physiol 589:3211-3229. CrossRef Medline
17. Esteban JA, Shi SH, Wilson C, Nuriya M, Huganir RL, Malinow R (2003) PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat Neurosci 6:136-143. CrossRef Medline
18. Faber ES, Sah P (2002) Physiological role of calcium-activated potassium currents in the rat lateral amygdala. J Neurosci 22:1618-1628. Medline
19. Fontanez-Nuin DE, Santini E, Quirk GJ, Porter JT (2011) Memory for fear extinction requires mGluR5-mediated activation of infralimbic neurons. Cereb Cortex 21:727-735. CrossRef Medline
20. Gabbott PL, Warner TA, Jays PR, Salway P, Busby SJ (2005) Prefrontal cortex in the rat: projections to subcortical autonomic, motor, and limbic centers. J Comp Neurol 492:145-177. CrossRef Medline
21. Herry C, Garcia R (2002) Prefrontal cortex long-term potentiation, but not long-term depression, is associated with the maintenance of extinction of learned fear in mice. J Neurosci 22:577-583. Medline
22. Herry C, Vouimba RM, Garcia R (1999) Plasticity in the mediodorsal thalamo-prefrontal cortical transmission in behaving mice. J Neurophysiol 82:2827-2832. Medline
23. Holmes A, Fitzgerald PJ, MacPherson KP, DeBrouse L, Colacicco G, Flynn SM, Masneuf S, Pleil KE, Li C, Marcinkiewcz CA, Kash TL, Gunduz-Cinar O, Camp M (2012) Chronic alcohol remodels prefrontal neurons and disrupts NMDAR-mediated fear extinction encoding. Nat Neurosci 15: 1359-1361. CrossRef Medline
24. Hu HJ, Alter BJ, Carrasquillo Y, Qiu CS, Gereau RW 4th (2007) Metabotropic glutamate receptor 5 modulates nociceptive plasticity via extracellular signal-regulated kinase-Kv4.2 signaling in spinal cord dorsal horn neurons. J Neurosci 27:13181-13191. CrossRef Medline
25. Hugues S, Chessel A, Lena I, Marsault R, Garcia R (2006) Prefrontal infusion of PD098059 immediately after fear extinction training blocks extinction-associated prefrontal synaptic plasticity and decreases prefrontal ERK2 phosphorylation. Synapse 60:280-287. CrossRef Medline
26. Kim JH, Li S, Richardson R (2011) Immunohistochemical analyses of longterm extinction of conditioned fear in adolescent rats. Cereb Cortex 21: 530-538. CrossRef Medline
27. Kim J, Lee S, Park H, Song B, Hong I, Geum D, Shin K, Choi S (2007a) Blockade of amygdala metabotropic glutamate receptor subtype 1 impairs fear extinction. Biochem Biophys Res Commun 355:188-193. CrossRef Medline
28. Kim J, Lee S, Park K, Hong I, Song B, Son G, Park H, Kim WR, Park E, Choe HK, Kim H, Lee C, Sun W, Kim K, Shin KS, Choi S (2007b) Amygdala depotentiation and fear extinction. Proc Natl Acad Sci U S A 104:20955-20960. CrossRef Medline
29. Kott S, Sager C, Tapken D, Werner M, Hollmann M (2009) Comparative analysis of the pharmacology of GluR1 in complex with transmembrane AMPA receptor regulatory proteins gamma2, gamma3, gamma4, and gamma8. Neuroscience 158:78-88. CrossRef Medline
30. Lee HK, Takamiya K, He K, Song L, Huganir RL (2010) Specific roles of AMPA receptor subunit GluR1 (GluA1) phosphorylation sites in regulating synaptic plasticity in the CA1 region of hippocampus. J Neurophysiol 103:479-489. CrossRef Medline
31. Lee JL, Milton AL, Everitt BJ (2006) Reconsolidation and extinction of conditioned fear: inhibition and potentiation. J Neurosci 26:5881-5887. CrossRef Medline
32. Lin HC, Mao SC, Su CL, Gean PW (2009) Alterations of excitatory transmission in the lateral amygdala during expression and extinction of fear memory. Int J Neuropsychopharmacol:1-11. CrossRef Medline
33. Lu YM, Jia Z, Janus C, Henderson JT, Gerlai R, Wojtowicz JM, Roder JC (1997) Mice lacking metabotropic glutamate receptor 5 show impaired learning and reduced CA1 long-term potentiation (LTP) but normal CA3 LTP. J Neurosci 17:5196-5205. Medline
34. Mamiya N, Fukushima H, Suzuki A, Matsuyama Z, Homma S, Frankland PW, Kida S (2009) Brain region-specific gene expression activation required for reconsolidation and extinction of contextual fear memory. J Neurosci 29:402-413. CrossRef Medline
35. McCallum J, Kim JH, Richardson R (2010) Impaired extinction retention in adolescent rats: effects of D-cycloserine. Neuropsychopharmacology 35: 2134-2142. CrossRef Medline
36. Milad MR, Quirk GJ (2002) Neurons in medial prefrontal cortex signal memory for fear extinction. Nature 420:70-74. CrossRef Medline
37. Milad MR, Quirk GJ (2012) Fear extinction as a model for translational neuroscience: ten years of progress. Annu Rev Psychol 63:129-151. CrossRef Medline
38. Mueller D, Porter JT, Quirk GJ (2008) Noradrenergic signaling in infralimbic cortex increases cell excitability and strengthens memory for fear extinction. J Neurosci 28:369-375. CrossRef Medline
39. Mueller D, Bravo-Rivera C, Quirk GJ (2010) Infralimbic D2 Receptors Are Necessary for Fear Extinction and Extinction-Related Tone Responses. Biol Psychiatry 68:1055-1060. CrossRef Medline
40. Orsini CA, Maren S (2012) Neural and cellular mechanisms of fear and extinction memory formation. Neurosci Biobehav Rev 36:1773-1802. CrossRef Medline
41. Pape HC, Paré D (2010) Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear. Physiol Rev 90:419-463. CrossRef Medline
42. Pattwell SS, Duhoux S, Hartley CA, Johnson DC, Jing D, Elliott MD, Ruberry EJ, Powers A, Mehta N, Yang RR, Soliman F, Glatt CE, Casey BJ, Ninan I, Lee FS (2012) Altered fear learning across development in both mouse and human. Proc Natl Acad Sci U S A 109:16318-16323. CrossRef Medline
43. Pfeiffer UJ, Fendt M (2006) Prefrontal dopamine D4 receptors are involved in encoding fear extinction. Neuroreport 17:847-850. CrossRef Medline
44. Phelps EA, LeDoux JE (2005) Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 48:175-187. CrossRef Medline
45. Power JM, Sah P (2007) Distribution of IP3-mediated calcium responses and their role in nuclear signalling in rat basolateral amygdala neurons. J Physiol 580:835-857. CrossRef Medline
46. Quirk GJ, Mueller D (2008) Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 33:56-72. CrossRef Medline
47. Quirk GJ, Likhtik E, Pelletier JG, Paré D (2003) Stimulation of medial prefrontal cortex decreases the responsiveness of central amygdala output neurons. J Neurosci 23:8800-8807. Medline
48. Quirk GJ, Garcia R, Gonzalez-Lima F (2006) Prefrontal mechanisms in extinction of conditioned fear. Biol Psychiatry 60:337-343. CrossRef Medline
49. Rodrigues SM, Bauer EP, Farb CR, Schafe GE, LeDoux JE (2002) The group I metabotropic glutamate receptor mGluR5 is required for fear memory formation and long-term potentiation in the lateral amygdala. J Neurosci 22:5219-5229. Medline
50. Rozov A, Burnashev N (1999) Polyamine-dependent facilitation of postsynaptic AMPA receptors counteracts paired-pulse depression. Nature 401:594-598. CrossRef Medline
51. Santini E, Quirk GJ, Porter JT (2008) Fear conditioning and extinction differentially modify the intrinsic excitability of infralimbic neurons. J Neurosci 28:4028-4036. CrossRef Medline
52. Santini E, Sepulveda-Orengo M, Porter JT (2012) Muscarinic receptors modulate the intrinsic excitability of infralimbic neurons and consolidation of fear extinction. Neuropsychopharmacology 37:2047-2056. CrossRef Medline
53. Schafe GE, Doyere V, LeDoux JE (2005) Tracking the fear engram: the lateral amygdala is an essential locus of fear memory storage. J Neurosci 25:10010-10014. CrossRef Medline
54. Sierra-Mercado D, Padilla-Coreano N, Quirk GJ (2011) Dissociable roles of prelimbic and infralimbic cortices, ventral hippocampus, and basolateral amygdala in the expression and extinction of conditioned fear. Neuropsychopharmacology 36:529-538. CrossRef Medline
55. Sourdet V, Russier M, Daoudal G, Ankri N, Debanne D (2003) Long-term enhancement of neuronal excitability and temporal fidelity mediated by metabotropic glutamate receptor subtype 5. J Neurosci 23:10238-10248. Medline
56. Spear LP (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24:417-463. CrossRef Medline
57. Swanson GT, Kamboj SK, Cull-Candy SG (1997) Single-channel properties of recombinant AMPA receptors depend on RNA editing, splice variation, and subunit composition. J Neurosci 17:58-69. Medline
58. Van den Oever MC, Goriounova NA, Li KW, Van der Schors RC, Binnekade R, Schoffelmeer AN, Mansvelder HD, Smit AB, Spijker S, De Vries TJ (2008) Prefrontal cortex AMPA receptor plasticity is crucial for cueinduced relapse to heroin-seeking. Nat Neurosci 11:1053-1058. CrossRef Medline
59. Verpelli C, Dvoretskova E, Vicidomini C, Rossi F, Chiappalone M, Schoen M, Di Stefano B, Mantegazza R, Broccoli V, Bockers TM, Dityatev A, Sala C (2011) Importance of Shank3 protein in regulating metabotropic glutamate receptor 5 (mGluR5) expression and signaling at synapses. J Biol Chem 286:34839-34850. CrossRef Medline
60. Vertes RP, Hoover WB, Viana Di Prisco G (2004) Theta rhythm of the hippocampus: subcortical control and functional significance. Behav Cogn Neurosci Rev 3:173-200. CrossRef Medline
61. Vikman KS, Rycroft BK, Christie MJ (2008) Switch to Ca2+-permeable AMPAand reduced NR2BNMDAreceptor-mediated neurotransmission at dorsal horn nociceptive synapses during inflammatory pain in the rat. J Physiol 586:515-527. CrossRef Medline
62. Viosca J, Lopez de Armentia M, Jancic D, Barco A (2009) Enhanced CREBdependent 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. CrossRef Medline
63. Wang H, Storm DR (2003) Calmodulin-regulated adenylyl cyclases: crosstalk and plasticity in the central nervous system. Mol Pharmacol 63:463-468. CrossRef Medline
64. Wang H, Wu LJ, Zhang F, Zhuo M (2008) Roles of calcium-stimulated adenylyl cyclase and calmodulin-dependent protein kinase IV in the regulation ofFMRPby group I metabotropic glutamate receptors. J Neurosci 28:4385-4397. CrossRef Medline
65. Wiltgen BJ, Royle GA, Gray EE, Abdipranoto A, Thangthaeng N, Jacobs N, Saab F, Tonegawa S, Heinemann SF, O'Dell TJ, Fanselow MS, Vissel B (2010) A role for calcium-permeable AMPA receptors in synaptic plasticity and learning. PLoS One 5.
66. Xu H, Wu LJ, Wang H, Zhang X, Vadakkan KI, Kim SS, Steenland HW, Zhuo M (2008) Presynaptic and postsynaptic amplifications of neuropathic pain in the anterior cingulate cortex. J Neurosci 28:7445-7453. CrossRef Medline
67. Xu J, Zhu Y, Contractor A, Heinemann SF (2009) mGluR5 has a critical role in inhibitory learning. J Neurosci 29:3676-3684. CrossRef Medline
68. Zhou Y, Won J, Karlsson MG, Zhou M, Rogerson T, Balaji J, Neve R, Poirazi P, Silva AJ (2009) CREB regulates excitability and the allocation of memory to subsets of neurons in the amygdala. Nat Neurosci 12:1438-1443. CrossRef Medline