Activity-dependent regulation of inhibitory synaptic transmission in hippocampal neurons

Nature Neuroscience

Volumn 9, Issue 5, 2006, Pages 642-649

  Hartman, Kenichi N ^a   Pal, Sumon K ^a   Burrone, Juan ^a,b   Murthy, Venkatesh N ^a  

^a HARVARD UNIVERSITY   (United States)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; CELL ACTIVITY; CONTROLLED STUDY; GABAERGIC SYSTEM; GABAERGIC TRANSMISSION; HIPPOCAMPUS; HYPERPOLARIZATION; INHIBITORY POSTSYNAPTIC POTENTIAL; NERVE CELL; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NEWBORN; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; RAT; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION;

ANIMALS; ANIMALS, NEWBORN; CARRIER PROTEINS; CELLS, CULTURED; DRUG INTERACTIONS; ELECTRIC STIMULATION; GLUTAMATE DECARBOXYLASE; HIPPOCAMPUS; ISOENZYMES; MEMBRANE POTENTIALS; MEMBRANE PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; NEURAL INHIBITION; NEURONS; PATCH-CLAMP TECHNIQUES; PHOSPHINIC ACIDS; POTASSIUM CHANNELS, INWARDLY RECTIFYING; PYRIDINES; RATS; SYNAPTIC TRANSMISSION; TETRODOTOXIN; TRANSFECTION; VESICULAR GLUTAMATE TRANSPORT PROTEIN 1;

EID: 33646850960     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1677     Document Type: Article

References (48)

1. Burrone, J. & Murthy, V.N. Synaptic gain control and homeostasis. Curr. Opin. Neurobiol. 13, 560-567 (2003).
2. Turrigiano, G.G. & Nelson, S.B. Homeostatic plasticity in the developing nervous system. Nat. Rev. Neurosci. 5, 97-107 (2004).
3. Davis, G.W. & Bezprozvanny, I. Maintaining the stability of neural function: a homeostatic hypothesis. Annu. Rev. Physiol. 63, 847-869 (2001).
4. Malinow, R. & Malenka, R.C. AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 25, 103-126 (2002).
5. Burrone, J., O'Byrne, M. & Murthy, V.N. Multiple forms of synaptic plasticity triggered by selective suppression of activity in individual neurons. Nature 420, 414-418 (2002).
6. Paradis, S., Sweeney, S.T. & Davis, G.W. Homeostatic control of presynapti release is triggered by postsynaptic membrane depolarization. Neuron 30, 737-749 (2001).
7. Benson, D.U., Isackson, P.J., Hendry, S.H. & Jones, E.G. Expression of glutamic acid decarboxylase mRNA in normal and monocularly deprived cat visual cortex. Brain Res. Mol. Brain Res. 5, 279-287 (1989).
8. Hendry, S.H. & Jones, E.G. Activity-dependent regulation of GABA expression in the visual cortex of adult monkeys. Neuron 1, 701-712 (1988).
9. Hensch, T.K. Critical period regulation. Annu. Rev. Neurosci. 27, 549-579 (2004).
10. Huang, Z.J. et al. BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 98, 739-755 (1999).
11. Gianfranceschi, L. et al. Visual cortex is rescued from the effects of dark rearing by overexpression of BDNF. Proc. Natl. Acad. Sci. USA 100, 12486-12491 (2003).
12. Maffei, A., Nelson, S.B. & Turrigiano, G.G. Selective reconfiguration of layer 4 visual cortical circuitry by visual deprivation. Nat. Neurosci. 7, 1353-1359 (2004).
13. Morales, B., Choi, S.Y. & Kirkwood, A. Dark rearing alters the development of GABAergic transmission in visual cortex. J. Neurosci. 22, 8084-8090 (2002).
14. Marty, S., Wehrle, R. & Sotelo, C. 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 (2000).
15. Seil, F.J. & Drake-Baumann, R. Reduced cortical inhibitory synaptogenesis in organotypic cerebellar cultures developing in the absence of neuronal activity. J. Comp. Neurol. 342, 366-377 (1994).
16. Seil, F.J. & Drake-Baumann, R. TrkB receptor ligands promote activity-dependent inhibitory synaptogenesis. J. Neurosci. 20, 5367-5373 (2000).
17. Chattopadhyaya, B. et al. Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. J. Neurosci. 24, 9598-9611 (2004).
18. Rosato-Siri, M., Grandolfo, M. & Ballerini, L. Activity-dependent modulation of GABAergic synapses in developing rat spinal networks in vitro. Eur. J. Neurosci. 16, 2123-2135 (2002).
19. Rutherford, L.C., DeWan, A., Lauer, H.M. &Turrigiano, G.G. Brain-derived neurotrophic factor mediates the activity-dependent regulation of inhibition in neocortical cultures. J. Neurosci. 17, 4527-4535 (1997).
20. Kilman, V., van Rossum, M.C. & Turrigiano, G.G. Activity deprivation reduces miniature IPSC amplitude by decreasing the number of postsynaptic GABA(A) receptors clustered at neocortical synapses. J. Neurosci. 22, 1328-1337 (2002).
21. Bellocchio, E.E., Reimer, R.J., Fremeau, R.T., Jr. & Edwards, R.H. Uptake of glutamate into synaptic vesicles by an inorganic phosphate transporter. Science 289, 957-960 (2000).
22. Kanaani, J. et al. A combination of three distinct trafficking signals mediates axonal targeting and presynaptic clustering of GAD65. J. Cell Biol. 158, 1229-1238 (2002).
23. McIntire, S.L., Reimer, R.J., Schuske, K., Edwards, R.H. & Jorgensen, E.M. Identification and characterization of the vesicular GABA transporter. Nature 389, 870-876 (1997).
24. Chaudhry, F.A. et al. The vesicular GABA transporter, VGAT, localizes to synaptic vesicles in sets of glycinergic as well as GABAergic neurons. J. Neurosci. 18, 9733-9750 (1998).
25. Owens, D.F., Boyce, L.H., Davis, M.B. & Kriegstein, A.R. Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramicidin perforated-patch recordings and calcium imaging. J. Neurosci. 16, 6414-6423 (1996).
26. Ebihara, S., Shirato, K., Harata, N. & Akaike, N. Gramicidin-perforated patch recording: GABA response in mammalian neurones with intact intracellular chloride. J. Physiol. (Lond.) 484, 77-86 (1995).
27. Ben-Ari, Y. Excitatory actions of gaba during development: the nature of the nurture. Nat. Rev. Neurosci. 3, 728-739 (2002).
28. Sigworth, F.J. The variance of sodium current fluctuations at the node of Ranvier. J. Physiol. (Lond.) 307, 97-129 (1980).
29. Auger, C. & Marty, A. Heterogeneity of functional synaptic parameters among single release sites. Neuron 19, 139-150 (1997).
30. Barberis, A., Petrini, E.M. & Cherubini, E. Presynaptic source of quantal size variability at GABAergic synapses in rat hippocampal neurons in culture. Eur. J. Neurosci. 20, 1803-1810 (2004).
31. Mangan, P.S. et al. Cultured hippocampal pyramidal neurons express two kinds of GABAA receptors. Mol. Pharmacol. 67, 775-788 (2005).
32. Jones, M.V., Jonas, P., Sahara, Y. & Westbrook, G.L. Microscopic kinetics and energetics distinguish GABAA receptor agonists from antagonists. Biophys. J. 81, 2660-2670 (2001).
33. Barberis, A., Lu, C., Vicini, S. & Mozrzymas, J.W. Developmental changes of GABA synaptic transient in cerebellar granule cells. Mol. Pharmacol. 67, 1221-1228 (2005).
34. Otis, T.S., De Koninck, Y. & Mody, I. Lasting potentiation of inhibition is associated with an increased number of gamma-aminobutyric acid type A receptors activated during miniature inhibitory postsynaptic currents. Proc. Natl. Acad. Sci. USA 91, 7698-7702 (1994).
35. Marty, S., Wehrle, R., Fritschy, J.M. & Sotelo, C. Quantitative effects produced by modifications of neuronal activity on the size of GABAA receptor clusters in hippocampal slice cultures. Eur. J. Neurosci. 20, 427-440 (2004).
36. Gaiarsa, J.L., Caillard, O. & Ben-Ari, Y. Long-term plasticity at GABAergic and glycinergic synapses: mechanisms and functional significance. Trends Neurosci. 25, 564-570 (2002).
37. Elmariah, S.B., Crumling, M.A., Parsons, T.D. & Balice-Gordon, R.J. Postsynaptic TrkB-mediated signaling modulates excitatory and inhibitory neurotransmitter receptor clustering at hippocampal synapses. J. Neurosci. 24, 2380-2393 (2004).
38. Genoud, C., Knott, G.W., Sakata, K., Lu, B. & Welker, E. Altered synapse formation in the adult somatosensory cortex of brain-derived neurotrophic factor heterozygote mice. J. Neurosci. 24, 2394-2400 (2004).
39. Lu, B. BDNF and activity-dependent synaptic modulation. Learn. Mem. 10, 86-98 (2003).
40. McLean Bolton, M., Pittman, A.J. & Lo, D.C. Brain-derived neurotrophic factor differentially regulates excitatory and inhibitory synaptic transmission in hippocampal cultures. J. Neurosci. 20, 3221-3232 (2000).
41. Ohba, S. et al. BDNF locally potentiates GABAergic presynaptic machineries: target-selective circuit inhibition. Cereb. Cortex 15, 291-298 (2005).
42. Rutherford, L.C., Nelson, S.B. & Turrigiano, G.G. BDNF has opposite effects on the quantal amplitude of pyramidal neuron and interneuron excitatory synapses. Neuron 21, 521-530 (1998).
43. Vicario-Abejon, C., Owens, D., McKay, R. & Segal, M. Role of neurotrophins in central synapse formation and stabilization. Nat. Rev. Neurosci. 3, 965-974 (2002).
44. Ernfors, P., Wetmore, C., Olson, L. & Persson, H. Identification of cells in rat brain and peripheral tissues expressing mRNA for members of the nerve growth factor family. Neuron 5, 511-526 (1990).
45. De Gois, S. et al. Homeostatic scaling of vesicular glutamate and GABA transporter expression in rat neocortical circuits. J. Neurosci. 25, 7121-7133 (2005).
46. Kittler, J.T. & Moss, S.J. Modulation of GABAA receptor activity by phosphorylation and receptor trafficking: implications for the efficacy of synaptic inhibition. Curr. Opin. Neurobiol. 13, 341-347 (2003).
47. Li, Z. & Murthy, V.N. Visualizing post-endocytic traffic of synaptic vesicles at hippocampal synapses. Neuron 31, 593-605 (2001).
48. Xu, X. & Shrager, P. Dependence of axon initial segment formation on Na+ channel expression. J. Neurosci. Res. 79, 428-441 (2005).