Initiation, labile, and stabilization phases of experience-dependent plasticity at neocortical synapses

Journal of Neuroscience

Volumn 33, Issue 19, 2013, Pages 8483-8493

  Wen, Jing A ^a   DeBlois, Mark C ^a,b   Barth, Alison L ^a  

^a CARNEGIE MELLON UNIVERSITY   (United States)

^b MARSHALL UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

METABOTROPIC RECEPTOR 5; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DEPRESSION; MEMBRANE STABILIZATION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SOMATOSENSORY CORTEX; SYNAPSE; SYNAPTIC POTENTIAL;

AFFERENT PATHWAYS; ANESTHETICS, LOCAL; ANIMALS; ANIMALS, NEWBORN; BIOPHYSICS; CENTRAL NERVOUS SYSTEM STIMULANTS; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GREEN FLUORESCENT PROTEINS; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEOCORTEX; NEURONAL PLASTICITY; NEURONS; PATCH-CLAMP TECHNIQUES; PICROTOXIN; SENSORY DEPRIVATION; TETRODOTOXIN; TIME FACTORS; VIBRISSAE;

EID: 84877272870     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3575-12.2013     Document Type: Article

References (55)

1. Abraham WC, Tate WP (1997) Metaplasticity: a new vista across the field of synaptic plasticity. Prog Neurobiol 52:303-323.CrossRef Medline
2. Anderson JJ, Bradbury MJ, Giracello DR, Chapman DF, Holtz G, Roppe J, King C, Cosford ND, Varney MA (2003) In vivo receptor occupancy of mGlu5 receptor antagonists using the novel radioligand [3H]3-methoxy- 5-(pyridin-2-ylethynyl)pyridine). Eur J Pharmacol 473:35-40.CrossRef Medline
3. Barrionuevo G, Schottler F, Lynch G (1980) The effects of repetitive low frequency stimulation on control and "potentiated" synaptic responses in the hippocampus. Life Sci 27:2385-2391.CrossRef Medline
4. Barth AL, Gerkin RC, Dean KL (2004) Alteration of neuronal firing properties after in vivo experience in a FosGFP transgenic mouse. J Neurosci 24:6466-6475.CrossRef Medline
5. Bashir ZI, Collingridge GL (1994) An investigation of depotentiation of long-term potentiation in the CA1 region of the hippocampus. Experimental brain research. Exp Brain Res 100:437-443.CrossRef Medline
6. Bear MF (1995) Mechanism for a sliding synaptic modification threshold. Neuron 15:1-4.CrossRef Medline
7. Bender KJ, Allen CB, Bender VA, Feldman DE (2006) Synaptic basis for whisker deprivation-induced synaptic depression in rat somatosensory cortex. J Neurosci 26:4155-4165.CrossRef Medline
8. Benedetti BL, Glazewski S, Barth AL (2009) Reliable and precise neuronal firing during sensory plasticity in superficial layers of primary somatosensory cortex. J Neurosci 29:11817-11827.CrossRef Medline
9. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289-300.
10. Benusková L, Diamond ME, Ebner FF (1994) Dynamic synaptic modification threshold: computational model of experience-dependent plasticity in adult rat barrel cortex. Proc Natl Acad Sci U S A 91:4791-4795.CrossRef Medline
11. Bienenstock EL, Cooper LN, Munro PW (1982) Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci 2:32-48.Medline
12. Brasier DJ, Feldman DE (2008) Synapse-specific expression of functional presynaptic NMDA receptors in rat somatosensory cortex. J Neurosci 28:2199-2211.CrossRef Medline
13. Clem RL, Barth A (2006) Pathway-specific trafficking of native AMPARs by in vivo experience. Neuron 49:663-670.CrossRef Medline
14. Clem RL, Celikel T, Barth AL (2008) Ongoing in vivo experience triggers synaptic metaplasticity in the neocortex. Science 319:101-104.CrossRef Medline
15. 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
16. Crair MC, Malenka RC (1995) A critical period for long-term potentiation at thalamocortical synapses. Nature 375:325-328.CrossRef Medline
17. Dachtler J, Hardingham NR, Glazewski S, Wright NF, Blain EJ, Fox K (2011) Experience-dependent plasticity acts via GluR1 and a novel neuronal nitric oxide synthase-dependent synaptic mechanism in adult cortex. J Neurosci 31:11220-11230.CrossRef Medline
18. Desai NS, Cudmore RH, Nelson SB, Turrigiano GG (2002) Critical periods for experience-dependent synaptic scaling in visual cortex. Nat Neurosci 5:783-789.Medline
19. Dudai Y (2004) The neurobiology of consolidations, or, how stable is the engram? Annu Rev Psychol 55:51-86.CrossRef Medline
20. Dudek SM, Bear MF (1992) Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc Natl Acad Sci U S A 89:4363-4367.CrossRef Medline
21. Feldman DE, Brecht M (2005) Map plasticity in somatosensory cortex. Science 310:810-815.CrossRef Medline
22. Feldman DE, Nicoll RA, Malenka RC, Isaac JT (1998) Long-term depression at thalamocortical synapses in developing rat somatosensory cortex. Neuron 21:347-357.CrossRef Medline
23. Finnerty GT, Roberts LS, Connors BW (1999) Sensory experience modifies the short-term dynamics of neocortical synapses. Nature 400:367-371.CrossRef Medline
24. Fujii S, Saito K, Miyakawa H, Ito K, Kato H (1991) Reversal of long-term potentiation (depotentiation) induced by tetanus stimulation of the input to CA1 neurons of guinea pig hippocampal slices. Brain Res 555:112-122.CrossRef Medline
25. Glazewski S, Benedetti BL, Barth AL (2007) Ipsilateral whiskers suppress experience-dependent plasticity in the barrel cortex. J Neurosci 27:3910-3920.CrossRef Medline
26. Goda Y, Stevens CF (1994) Two components of transmitter release at a central synapse. Proc Natl Acad Sci U S A 91:12942-12946.CrossRef Medline
27. Hardingham N, Wright N, Dachtler J, Fox K (2008) Sensory deprivation unmasks a PKA-dependent synaptic plasticity mechanism that operates in parallel with CaMKII. Neuron 60:861-874.CrossRef Medline
28. Hensch TK (2005) Critical period plasticity in local cortical circuits. Nat Rev Neurosci 6:877-888.CrossRef Medline
29. Hou Q, Gilbert J, Man HY (2011) Homeostatic regulation of AMPA receptor trafficking and degradation by light-controlled single-synaptic activation. Neuron 72:806-818.CrossRef Medline
30. Jacob V, Petreanu L, Wright N, Svoboda K, Fox K (2012) Regular spiking and intrinsic bursting pyramidal cells show orthogonal forms of experience-dependent plasticity in layer V of barrel cortex. Neuron 73: 391-404.CrossRef Medline
31. Jiao Y, Zhang C, Yanagawa Y, Sun QQ (2006) Major effects of sensory experiences on the neocortical inhibitory circuits. J Neurosci 26:8691-8701.CrossRef Medline
32. Kirkwood A, Dudek SM, Gold JT, Aizenman CD, Bear MF (1993) Common forms of synaptic plasticity in the hippocampus and neocortex in vitro. Science 260:1518-1521.CrossRef Medline
33. Kirkwood A, Lee HK, Bear MF (1995) Co-regulation of long-term potentiation and experience-dependent synaptic plasticity in visual cortex by age and experience. Nature 375:328-331.CrossRef Medline
34. Mahan AL, Ressler KJ (2012) Fear conditioning, synaptic plasticity and the amygdala: implications for posttraumatic stress disorder. Trends Neurosci 35:24-35.CrossRef Medline
35. Malenka RC, Bear MF (2004) LTP and LTD: an embarrassment of riches. Neuron 44:5-21.CrossRef Medline
36. McClelland JL (1998) Complementary learning systems in the brain. A connectionist approach to explicit and implicit cognition and memory. Ann N Y Acad Sci 843:153-169.CrossRef Medline
37. Monfils MH, Cowansage KK, Klann E, LeDoux JE (2009) Extinctionreconsolidation boundaries: key to persistent attenuation of fear memories. Science 324:951-955.CrossRef Medline
38. Myers KM, Ressler KJ, DavisM (2006) Different mechanisms of fear extinction dependent on length of time since fear acquisition. Learn Mem 13: 216-223.CrossRef Medline
39. Nader K, Schafe GE, LeDoux JE (2000) The labile nature of consolidation theory. Nat Rev Neurosci 1:216-219.CrossRef Medline
40. O'Brien RJ, Kamboj S, Ehlers MD, Rosen KR, Fischbach GD, Huganir RL (1998) Activity-dependent modulation of synaptic AMPA receptor accumulation. Neuron 21:1067-1078.CrossRef Medline
41. Philpot BD, Espinosa JS, Bear MF (2003) Evidence for altered NMDA receptor function as a basis for metaplasticity in visual cortex. J Neurosci 23:5583-5588.Medline
42. Philpot BD, Cho KK, Bear MF (2007) Obligatory role of NR2A for metaplasticity in visual cortex. Neuron 53:495-502.CrossRef Medline
43. Qi Y, Hu NW, Rowan MJ (2013) Switching off LTP: mGlu and NMDA receptor-dependent novelty exploration-induced depotentiation in the rat hippocampus. Cereb Cortex 23:932-939.CrossRef Medline
44. Rodríguez-Moreno A, Paulsen O (2008) Spike timing-dependent longterm depression requires presynaptic NMDA receptors. Nat Neurosci 11:744-745.CrossRef Medline
45. Sutton MA, Wall NR, Aakalu GN, Schuman EM (2004) Regulation of den-dritic protein synthesis by miniature synaptic events. Science 304:1979-1983.CrossRef Medline
46. Takahashi T, Svoboda K, Malinow R (2003) Experience strengthening transmission by driving AMPA receptors into synapses. Science 299: 1585-1588.CrossRef Medline
47. Turrigiano GG, Leslie KR, Desai NS, Rutherford LC, Nelson SB (1998) Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391:892-896.CrossRef Medline
48. Villarreal DM, Do V, Haddad E, Derrick BE (2002) NMDA receptor antagonists sustain LTP and spatial memory: active processes mediate LTP decay. Nat Neurosci 5:48-52.CrossRef Medline
49. Wen JA, Barth AL (2011) Input-specific critical periods for experiencedependent plasticity in layer 2/3 pyramidal neurons. J Neurosci 31: 4456-4465.CrossRef Medline
50. Wen JA, Barth AL (2012) Synaptic lability after experience-dependent plasticity is not mediated by calcium-permeable AMPARs. Front Mol Neurosci 5:15.Medline
51. Whitlock JR, Heynen AJ, Shuler MG, Bear MF (2006) Learning induces long-term potentiation in the hippocampus. Science 313:1093-1097.CrossRef Medline
52. Wiltgen BJ, Brown RA, Talton LE, Silva AJ (2004) New circuits for old memories: the role of the neocortex in consolidation. Neuron 44:101-108.CrossRef Medline
53. Xu L, Anwyl R, Rowan MJ (1998) Spatial exploration induces a persistent reversal of long-term potentiation in rat hippocampus. Nature 394: 891-894.CrossRef Medline
54. Xu-Friedman MA, RegehrWG (1999) Presynaptic strontium dynamics and synaptic transmission. Biophys J 76:2029-2042.CrossRef Medline
55. Zhou Q, Tao HW, Poo MM (2003) Reversal and stabilization of synaptic modifications in a developing visual system. Science 300: 1953-1957.CrossRef Medline