Postsynaptic spiking homeostatically induces cell-autonomous regulation of inhibitory inputs via retrograde signaling

Journal of Neuroscience

Volumn 30, Issue 48, 2010, Pages 16220-16231

  Peng, Yi Rong ^a,b   Zeng, Si Yu ^a,b   Song, He Ling ^a   Li, Min Yin ^a,b   Yamada, Maki K ^c,d   Yu, Xiang ^a  

^a Shanghai Jiao Tong University Affiliated Sixth People s Hospital   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR ALPHA1; BRAIN DERIVED NEUROTROPHIC FACTOR; CAPSAICIN; GLUTAMATE DECARBOXYLASE 65; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR2.1; KAINIC ACID; VANILLOID RECEPTOR 1; VESICULAR INHIBITORY AMINO ACID TRANSPORTER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EXCITATORY POSTSYNAPTIC POTENTIAL; GABAERGIC TRANSMISSION; HIPPOCAMPUS; HOMEOSTASIS; IMMUNOCYTOCHEMISTRY; INHIBITORY POSTSYNAPTIC POTENTIAL; NONHUMAN; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; RAT; SCAVENGING SYSTEM; SPIKE WAVE; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; CELLS, CULTURED; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; HOMEOSTASIS; NEURAL INHIBITION; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 78649757879     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3085-10.2010     Document Type: Article

References (55)

1. Abbott LF, Nelson SB (2000) Synaptic plasticity: taming the beast. Nat Neurosci 3 [Suppl]:1178-1183.
2. Applied Biosystems (2001) User bulletin no. 2, Rev B. Foster City, CA: Applied Biosystems.
3. Ben-Ari Y (1985) Limbic seizure and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy. Neuroscience 14:375-403.
4. Ben-Ari Y (2008) Epilepsies and neuronal plasticity: for better or for worse? Dialogues Clin Neurosci 10:17-27.
5. Bi G, Poo M (2001) Synaptic modification by correlated activity: Hebb's postulate revisited. Annu Rev Neurosci 24:139-166.
6. Bolton MM, Pittman AJ, Lo DC (2000) Brain-derived neurotrophic factor differentially regulates excitatory and inhibitory synaptic transmission in hippocampal cultures. J Neurosci 20:3221-3232.
7. Burrone J, Murthy VN (2003) Synaptic gain control and homeostasis. Curr Opin Neurobiol 13:560-567.
8. Burrone J, O'Byrne M, Murthy VN (2002) Multiple forms of synaptic plasticity triggered by selective suppression of activity in individual neurons. Nature 420:414-418.
9. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389:816-824.
10. Davis GW (2006) Homeostatic control of neural activity: from phenomenology to molecular design. Annu Rev Neurosci 29:307-323.
11. Davis GW, DiAntonio A, Petersen SA, Goodman CS (1998) Postsynaptic PKA controls quantal size and reveals a retrograde signal that regulates presynaptic transmitter release in Drosophila. Neuron 20:305-315.
12. De Gois S, Schäfer MK, Defamie N, Chen C, Ricci A, Weihe E, Varoqui H, Erickson JD (2005) Homeostatic scaling of vesicular glutamate and GABA transporter expression in rat neocortical circuits. J Neurosci 25:7121-7133.
13. Erickson JD, De Gois S, Varoqui H, Schafer MK, Weihe E (2006) Activity-dependent regulation of vesicular glutamate and GABA transporters: a means to scale quantal size. Neurochem Int 48:643-649.
14. Gibson HE, Edwards JG, Page RS, Van Hook MJ, Kauer JA (2008) TRPV1 channels mediate long-term depression at synapses on hippocampal interneurons. Neuron 57:746-759.
15. Gonzalez M, Ruggiero FP, Chang Q, Shi YJ, Rich MM, Kraner S, Balice-Gordon RJ (1999) Disruption of Trkb-mediated signaling induces disassembly of postsynaptic receptor clusters at neuromuscular junctions. Neuron 24:567-583.
16. Hartman KN, Pal SK, Burrone J, Murthy VN (2006) Activity-dependent regulation of inhibitory synaptic transmission in hippocampal neurons. Nat Neurosci 9:642-649.
17. Hartmann M, Heumann R, Lessmann V (2001) Synaptic secretion of BDNF after high-frequency stimulation of glutamatergic synapses. EMBO J 20:5887-5897.
18. Holt JR, Johns DC, Wang S, Chen ZY, Dunn RJ, Marban E, Corey DP (1999) Functional expression of exogenous proteins in mammalian sensory hair cells infected with adenoviral vectors. J Neurophysiol 81:1881-1888.
19. Huang ZJ, Kirkwood A, Pizzorusso T, Porciatti V, Morales B, Bear MF, Maffei L, Tonegawa S (1999) BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 98:739-755.
20. Ibata K, Sun Q, Turrigiano GG (2008) Rapid synaptic scaling induced by changes in postsynaptic firing. Neuron 57:819-826.
21. Katz LC, Shatz CJ (1996) Synaptic activity and the construction of cortical circuits. Science 274:1133-1138.
22. Kauer JA, Gibson HE (2009) Hot flash: TRPV channels in the brain. Trends Neurosci 32:215-224.
23. Kilman V, van Rossum MC, Turrigiano GG (2002) Activity deprivation reduces miniature IPSC amplitude by decreasing the number of postsynaptic GABA(A) receptors clustered at neocortical synapses. J Neurosci 22:1328-1337.
24. Kohara K, Yasuda H, Huang Y, Adachi N, Sohya K, Tsumoto T (2007) A local reduction in cortical GABAergic synapses after a loss of endogenous brain-derived neurotrophic factor, as revealed by single-cell gene knockout method. J Neurosci 27:7234-7244.
25. Koizumi S, Contreras ML, Matsuda Y, Hama T, Lazarovici P, Guroff G (1988) K-252a: a specific inhibitor of the action of nerve growth factor on PC 12 cells. J Neurosci 8:715-721.
26. Kojima M, Takei N, Numakawa T, Ishikawa Y, Suzuki S, Matsumoto T, Katoh-Semba R, Nawa H, Hatanaka H (2001) Biological characterization and optical imaging of brain-derived neurotrophic factor-green fluorescent protein suggest an activity-dependent local release of brain-derived neurotrophic factor in neurites of cultured hippocampal neurons. J Neurosci Res 64:1-10.
27. Kubo Y, Baldwin TJ, Jan YN, Jan LY (1993) Primary structure and functional expression of a mouse inward rectifier potassium channel. Nature 362:127-133. (Pubitemid 23085250)
28. Kuczewski N, Porcher C, Lessmann V, Medina I, Gaiarsa JL (2009) Activity-dependent dendritic release of BDNF and biological consequences. Mol Neurobiol 39:37-49.
29. Lothman EW, Collins RC (1981) Kainic acid induced limbic seizures: metabolic, behavioral, electroencephalographic and neuropathological correlates. Brain Res 218:299-318.
30. Maffei A, Turrigiano GG (2008) Multiple modes of network homeostasis in visual cortical layer 2/3. J Neurosci 28:4377-4384.
31. Maffei A, Nelson SB, Turrigiano GG (2004) Selective reconfiguration of layer 4 visual cortical circuitry by visual deprivation. Nat Neurosci 7:1353-1359.
32. Marty S, Wehrlé R, Sotelo C (2000) Neuronal activity and brain-derived neurotrophic factor regulate the density of inhibitory synapses in organotypic slice cultures of postnatal hippocampus. J Neurosci 20:8087-8095.
33. Mody I (2005) Aspects of the homeostaic plasticity of GABAA receptor-mediated inhibition. J Physiol 562:37-46.
34. Murphy DD, Cole NB, Segal M (1998) Brain-derived neurotrophic factor mediates estradiol-induced dendritic spine formation in hippocampal neurons. Proc Natl Acad Sci U S A 95:11412-11417.
35. Ohba S, Ikeda T, Ikegaya Y, Nishiyama N, Matsuki N, Yamada MK (2005) BDNF locally potentiates GABAergic presynaptic machineries: target-selective circuit inhibition. Cereb Cortex 15:291-298.
36. Petersen SA, Fetter RD, Noordermeer JN, Goodman CS, DiAntonio A (1997) Genetic analysis of glutamate receptors in Drosophila reveals a retrograde signal regulating presynaptic transmitter release. Neuron 19:1237-1248.
37. Poo MM (2001) Neurotrophins as synaptic modulators. Nat Rev Neurosci 2:24-32.
38. Regehr WG, Carey MR, Best AR (2009) Activity-dependent regulation of synapses by retrograde messengers. Neuron 63:154-170.
39. Rich MM, Wenner P (2007) Sensing and expressing homeostatic synaptic plasticity. Trends Neurosci 30:119-125.
40. Swanwick CC, Murthy NR, Kapur J (2006) Activity-dependent scaling of GABAergic synapse strength is regulated by brain-derived neurotrophic factor. Mol Cell Neurosci 31:481-492.
41. Tapley P, Lamballe F, Barbacid M (1992) K252a is a selective inhibitor of the tyrosine protein kinase activity of the trk family of oncogenes and neurotrophin receptors. Oncogene 7:371-381.
42. Turrigiano GG (2008) The self-tuning neuron: synaptic scaling of excitatory synapses. Cell 135:422-435.
43. Turrigiano GG, Nelson SB (2004) Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci 5:97-107.
44. Turrigiano GG, Leslie KR, Desai NS, Rutherford LC, Nelson SB (1998) Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391:892-896.
45. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH (2002) Functional neurogenesis in the adult hippocampus. Nature 415:1030-1034.
46. Vicario-Abejón C, Owens D, McKay R, Segal M (2002) Role of neurotrophins in central synapse formation and stabilization. Nat Rev Neurosci 3:965-974.
47. Wang CL, Zhang L, Zhou Y, Zhou J, Yang XJ, Duan SM, Xiong ZQ, Ding YQ (2007) Activity-dependent development of callosal projections in the somatosensory cortex. J Neurosci 27:11334-11342.
48. Wetmore C, Olson L, Bean AJ (1994) Regulation of brain-derived neurotrophic factor (BDNF) expression and release from hippocampal neurons is mediated by non-NMDA type glutamate receptors. J Neurosci 14:1688-1700.
49. Yamada MK, Nakanishi K, Ohba S, Nakamura T, Ikegaya Y, Nishiyama N, Matsuki N (2002) Brain-derived neurotrophic factor promotes the maturation of GABAergic mechanisms in cultured hippocampal neurons. J Neurosci 22:7580-7585.
50. Yu LM, Goda Y (2009) Dendritic signalling and homeostatic adaptation. Curr Opin Neurobiol 19:327-335.
51. Yu X, Malenka RC (2003) Beta-catenin is critical for dendritic morphogenesis. Nat Neurosci 6:1169-1177.
52. Zemelman BV, Nesnas N, Lee GA, Miesenbock G (2003) Photochemical gating of heterologous ion channels: remote control over genetically designated populations of neurons. Proc Natl Acad Sci U S A 100:1352-1357.
53. Zhang X, Zhu J, Yang GY, Wang QJ, Qian L, Chen YM, Chen F, Tao Y, Hu HS, Wang T, Luo ZG (2007) Dishevelled promotes axon differentiation by regulating atypical protein kinase C. Nat Cell Biol 9:743-754.
54. Zhao L, Sheng AL, Huang SH, Yin YX, Chen B, Li XZ, Zhang Y, Chen ZY (2009) Mechanism underlying activity-dependent insertion of TrkB into the neuronal surface. J Cell Sci 122:3123-3136.
55. Zhou P, Porcionatto M, Pilapil M, Chen Y, Choi Y, Tolias KF, Bikoff JB, Hong EJ, Greenberg ME, Segal RA (2007) Polarized signaling endosomes coordinate BDNF-induced chemotaxis of cerebellar precursors. Neuron 55:53-68.