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Neural Plasticity
Volume 2011, Article ID 489470, 6 pages
http://dx.doi.org/10.1155/2011/489470
Review Article

Mechanisms of GABAergic Homeostatic Plasticity

Department of Physiology, Emory University, School of Medicine, 615 Michael Street, Room 601, Atlanta, GA 30322, USA

Received 1 March 2011; Accepted 25 April 2011

Academic Editor: Evelyne Sernagor

Copyright © 2011 Peter Wenner. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. M. Fritschy, “Epilepsy, E/I balance and GABA(A) receptor plasticity,” Frontiers in Molecular Neuroscience, vol. 1, p. 5, 2008. View at Google Scholar
  2. I. Mody, “Aspects of the homeostaic plasticity of GABA receptor-mediated inhibition,” Journal of Physiology, vol. 562, no. 1, pp. 37–46, 2005. View at Publisher · View at Google Scholar · View at PubMed
  3. G. W. Davis, “Homeostatic control of neural activity: from phenomenology to molecular design,” Annual Review of Neuroscience, vol. 29, pp. 307–323, 2006. View at Publisher · View at Google Scholar · View at PubMed
  4. K. Pozo and Y. Goda, “Unraveling mechanisms of homeostatic synaptic plasticity,” Neuron, vol. 66, no. 3, pp. 337–351, 2010. View at Publisher · View at Google Scholar · View at PubMed
  5. M. M. Rich and P. Wenner, “Sensing and expressing homeostatic synaptic plasticity,” Trends in Neurosciences, vol. 30, no. 3, pp. 119–125, 2007. View at Publisher · View at Google Scholar · View at PubMed
  6. G. Turrigiano, “Too many cooks? Intrinsic and synaptic homeostatic mechanisms in cortical circuit refinement,” Annual Review of Neuroscience, vol. 34, 2011. View at Publisher · View at Google Scholar
  7. G. Turrigiano, L. F. Abbott, and E. Marder, “Activity-dependent changes in the intrinsic properties of cultured neurons,” Science, vol. 264, no. 5161, pp. 974–977, 1994. View at Google Scholar
  8. G. G. Turrigiano, K. R. Leslie, N. S. Desai, L. C. Rutherford, and S. B. Nelson, “Activity-dependent scaling of quantal amplitude in neocortical neurons,” Nature, vol. 391, no. 6670, pp. 892–896, 1998. View at Publisher · View at Google Scholar · View at PubMed
  9. J. Burrone, M. O'Byrne, and V. N. Murthy, “Multiple forms of synaptic plasticity triggered by selective suppression of activity in individual neurons,” Nature, vol. 420, no. 6914, pp. 414–418, 2002. View at Publisher · View at Google Scholar · View at PubMed
  10. V. Kilman, M. C. Van Rossum, and G. G. Turrigiano, “Activity deprivation reduces miniature IPSC amplitude by decreasing the number of postsynaptic GABA receptors clustered at neocortical synapses,” Journal of Neuroscience, vol. 22, no. 4, pp. 1328–1337, 2002. View at Google Scholar
  11. K. R. Leslie, S. B. Nelson, and G. G. Turrigiano, “Postsynaptic depolarization scales quantal amplitude in cortical pyramidal neurons,” The Journal of neuroscience, vol. 21, no. 19, article RC170, 2001. View at Google Scholar
  12. D. V. Lissin, S. N. Gomperts, R. C. Carroll et al., “Activity differentially regulates the surface expression of synaptic AMPA and NMDA glutamate receptors,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 12, pp. 7097–7102, 1998. View at Publisher · View at Google Scholar
  13. T. C. Thiagarajan, E. S. Piedras-Renteria, and R. W. Tsien, “α- and βCaMKII: inverse regulation by neuronal activity and opposing effects on synaptic strength,” Neuron, vol. 36, no. 6, pp. 1103–1114, 2002. View at Publisher · View at Google Scholar
  14. C. J. Wierenga, K. Ibata, and G. G. Turrigiano, “Postsynaptic expression of homeostatic plasticity at neocortical synapses,” Journal of Neuroscience, vol. 25, no. 11, pp. 2895–2905, 2005. View at Publisher · View at Google Scholar · View at PubMed
  15. S. H. Hendry, M. M. Huntsman, A. Vinuela, H. Mohler, A. L. De Blas, and E. G. Jones, “GABA(A) receptor subunit immunoreactivity in primate visual cortex: distribution in macaques and humans and regulation by visual input in adulthood,” Journal of Neuroscience, vol. 14, no. 4, pp. 2383–2401, 1994. View at Google Scholar
  16. S. H. Hendry and E. G. Jones, “Reduction in numbers of immunostained GABAergic neurones in deprived-eye dominance columns of monkey area 17,” Nature, vol. 320, no. 6064, pp. 750–753, 1986. View at Google Scholar
  17. C. Gonzalez-Islas and P. Wenner, “Spontaneous network activity in the embryonic spinal cord regulates AMPAergic and GABAergic synaptic strength,” Neuron, vol. 49, no. 4, pp. 563–575, 2006. View at Publisher · View at Google Scholar · View at PubMed
  18. K. N. Hartman, S. K. Pal, J. Burrone, and V. N. Murthy, “Activity-dependent regulation of inhibitory synaptic transmission in hippocampal neurons,” Nature Neuroscience, vol. 9, no. 5, pp. 642–649, 2006. View at Publisher · View at Google Scholar · View at PubMed
  19. J. Kim and B. E. Alger, “Reduction in endocannabinoid tone is a homeostatic mechanism for specific inhibitory synapses,” Nature Neuroscience, vol. 13, no. 5, pp. 592–600, 2010. View at Publisher · View at Google Scholar · View at PubMed
  20. Y. R. Peng, S. Y. Zeng, H. L. Song, M. Y. Li, M. K. Yamada, and X. Yu, “Postsynaptic spiking homeostatically induces cell-autonomous regulation of inhibitory inputs via retrograde signaling,” Journal of Neuroscience, vol. 30, pp. 16220–16231, 2010. View at Google Scholar
  21. C. C. Swanwick, N. R. Murthy, and J. Kapur, “Activity-dependent scaling of GABAergic synapse strength is regulated by brain-derived neurotrophic factor,” Molecular and Cellular Neuroscience, vol. 31, no. 3, pp. 481–492, 2006. View at Publisher · View at Google Scholar · View at PubMed
  22. J. Echegoyen, A. Neu, K. D. Graber, and I. Soltesz, “Homeostatic plasticity studied using in vivo hippocampal activity-blockade: synaptic scaling, intrinsic plasticity and age-dependence,” PloS One, vol. 2, no. 1, article e700, 2007. View at Google Scholar
  23. C. Gonzalez-Islas, N. Chub, and P. Wenner, “NKCC1 and AE3 appear to accumulate chloride in embryonic motoneurons,” Journal of Neurophysiology, vol. 101, no. 2, pp. 507–518, 2009. View at Publisher · View at Google Scholar · View at PubMed
  24. C. Gonzalez-Islas, N. Chub, M. A. Garcia-Bereguiain, and P. Wenner, “GABAergic synaptic scaling in embryonic motoneurons is mediated by a shift in the chloride reversal potential,” The Journal of Neuroscience, vol. 30, pp. 13016–13020, 2010. View at Google Scholar
  25. U. R. Karmarkar and D. V. Buonomano, “Different forms of homeostatic plasticity are engaged with distinct temporal profiles,” European Journal of Neuroscience, vol. 23, no. 6, pp. 1575–1584, 2006. View at Publisher · View at Google Scholar · View at PubMed
  26. Y. Ben-Ari, J. L. Gaiarsa, R. Tyzio, and R. Khazipov, “GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations,” Physiological Reviews, vol. 87, no. 4, pp. 1215–1284, 2007. View at Publisher · View at Google Scholar · View at PubMed
  27. P. Blaesse, M. S. Airaksinen, C. Rivera, and K. Kaila, “Cation-chloride cotransporters and neuronal function,” Neuron, vol. 61, no. 6, pp. 820–838, 2009. View at Publisher · View at Google Scholar · View at PubMed
  28. D. P. Bonislawski, E. P. Schwarzbach, and A. S. Cohen, “Brain injury impairs dentate gyrus inhibitory efficacy,” Neurobiology of Disease, vol. 25, no. 1, pp. 163–169, 2007. View at Publisher · View at Google Scholar · View at PubMed
  29. J. A. Coull, S. Beggs, D. Boudreau et al., “BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain,” Nature, vol. 438, no. 7070, pp. 1017–1021, 2005. View at Publisher · View at Google Scholar · View at PubMed
  30. J. A. Coull, D. Boudreau, K. Bachand et al., “Trans-synaptic shift in anion gradient in spinal lamina I neurons as a mechanism of neuropathic pain,” Nature, vol. 424, no. 6951, pp. 938–942, 2003. View at Publisher · View at Google Scholar · View at PubMed
  31. Y. De Koninck, “Altered chloride homeostasis in neurological disorders: a new target,” Current Opinion in Pharmacology, vol. 7, no. 1, pp. 93–99, 2007. View at Publisher · View at Google Scholar · View at PubMed
  32. J. Nabekura, T. Ueno, A. Okabe et al., “Reduction of KCC2 Expression and GABA Receptor-Mediated Excitation after In Vivo Axonal Injury,” Journal of Neuroscience, vol. 22, no. 11, pp. 4412–4417, 2002. View at Google Scholar
  33. B. B. Pond, K. Berglund, T. Kuner, G. Feng, G. J. Augustine, and R. D. Schwartz-Bloom, “The chloride transporter Na(+)-K(+)-Cl- cotransporter isoform-1 contributes to intracellular chloride increases after in vitro ischemia,” Journal of Neuroscience, vol. 26, no. 5, pp. 1396–1406, 2006. View at Publisher · View at Google Scholar · View at PubMed
  34. T. J. Price, F. Cervero, M. S. Gold, D. L. Hammond, and S. A. Prescott, “Chloride regulation in the pain pathway,” Brain Research Reviews, vol. 60, no. 1, pp. 149–170, 2009. View at Publisher · View at Google Scholar · View at PubMed
  35. C. Rivera, J. Voipio, and K. Kaila, “Two developmental switches in GABAergic signalling: the K+-Cl- cotransporter KCC2 and carbonic anhydrase CAVII,” Journal of Physiology, vol. 562, no. 1, pp. 27–36, 2005. View at Publisher · View at Google Scholar · View at PubMed
  36. C. Rivera, J. Voipio, J. Thomas-Crusells et al., “Mechanism of activity-dependent downregulation of the neuron-specific K-Cl cotransporter KCC2,” Journal of Neuroscience, vol. 24, no. 19, pp. 4683–4691, 2004. View at Publisher · View at Google Scholar · View at PubMed
  37. Y. Yan, R. J. Dempsey, A. Flemmer, B. Forbush, and D. Sun, “Inhibition of Na(+)-K(+)-Cl(-) cotransporter during focal cerebral ischemia decreases edema and neuronal damage,” Brain Research, vol. 961, no. 1, pp. 22–31, 2003. View at Publisher · View at Google Scholar
  38. P. Boulenguez, S. Liabeuf, R. Bos et al., “Down-regulation of the potassium-chloride cotransporter KCC2 contributes to spasticity after spinal cord injury,” Nat Med, no. 16, pp. 302–307, 2010. View at Google Scholar
  39. K. Chen, I. Aradi, N. Thon, M. Eghbal-Ahmadi, T. Z. Baram, and I. Soltesz, “Persistently modified h-channels after complex febrile seizures convert the seizure-induced enhancement of inhibition to hyperexcitability,” Nature Medicine, vol. 7, no. 3, pp. 331–337, 2001. View at Publisher · View at Google Scholar · View at PubMed
  40. K. Chen, T. Z. Baram, and I. Soltesz, “Febrile seizures in the developing brain result in persistent modification of neuronal excitability in limbic circuits,” Nature Medicine, vol. 5, no. 8, pp. 888–894, 1999. View at Publisher · View at Google Scholar · View at PubMed
  41. L. C. Rutherford, S. B. Nelson, and G. G. Turrigiano, “BDNF has opposite effects on the quantal amplitude of pyramidal neuron and interneuron excitatory synapses,” Neuron, vol. 21, no. 3, pp. 521–530, 1998. View at Publisher · View at Google Scholar
  42. M. C. Chang, J. M. Park, K. A. Pelkey et al., “Narp regulates homeostatic scaling of excitatory synapses on parvalbumin-expressing interneurons,” Nature Neuroscience, vol. 13, pp. 1090–1097, 2010. View at Publisher · View at Google Scholar
  43. S. Doyle, S. Pyndiah, S. De Gois, and J. D. Erickson, “Excitation-transcription coupling via calcium/calmodulin-dependent protein kinase/ERK1/2 signaling mediates the coordinate induction of VGLUT2 and Narp triggered by a prolonged increase in glutamatergic synaptic activity,” Journal of Biological Chemistry, vol. 285, no. 19, pp. 14366–14376, 2010. View at Publisher · View at Google Scholar · View at PubMed
  44. A. F. Bartley, Z. J. Huang, K. M. Huber, and J. R. Gibson, “Differential activity-dependent, homeostatic plasticity of two neocortical inhibitory circuits,” Journal of Neurophysiology, vol. 100, no. 4, pp. 1983–1994, 2008. View at Publisher · View at Google Scholar · View at PubMed
  45. N. S. Desai, L. C. Rutherford, and G. G. Turrigiano, “BDNF regulates the intrinsic excitability of cortical neurons,” Learning and Memory, vol. 6, no. 3, pp. 284–291, 1999. View at Google Scholar
  46. A. Maffei, S. B. Nelson, and G. G. Turrigiano, “Selective reconfiguration of layer 4 visual cortical circuitry by visual deprivation,” Nature Neuroscience, vol. 7, no. 12, pp. 1353–1359, 2004. View at Publisher · View at Google Scholar · View at PubMed
  47. A. Maffei and G. Turrigiano, “The age of plasticity: developmental regulation of synaptic plasticity in neocortical microcircuits,” Progress in Brain Research, vol. 169, pp. 211–223, 2008. View at Publisher · View at Google Scholar · View at PubMed
  48. A. Maffei, K. Nataraj, S. B. Nelson, and G. G. Turrigiano, “Potentiation of cortical inhibition by visual deprivation,” Nature, vol. 443, no. 7107, pp. 81–84, 2006. View at Publisher · View at Google Scholar · View at PubMed
  49. L. C. Rutherford, A. DeWan, H. M. Lauer, and G. G. Turrigiano, “Brain-derived neurotrophic factor mediates the activity-dependent regulation of inhibition in neocortical cultures,” Journal of Neuroscience, vol. 17, no. 12, pp. 4527–4535, 1997. View at Google Scholar
  50. J. C. Wilhelm, M. M. Rich, and P. Wenner, “Compensatory changes in cellular excitability, not synaptic scaling, contribute to homeostatic recovery of embryonic network activity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 16, pp. 6760–6765, 2009. View at Publisher · View at Google Scholar · View at PubMed
  51. J. C. Wilhelm and P. Wenner, “GABA transmission is a critical step in the process of triggering homeostatic increases in quantal amplitude,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 32, pp. 11412–11417, 2008. View at Publisher · View at Google Scholar · View at PubMed
  52. N. S. Desai, R. H. Cudmore, S. B. Nelson, and G. G. Turrigiano, “Critical periods for experience-dependent synaptic scaling in visual cortex,” Nature Neuroscience, vol. 5, no. 8, pp. 783–789, 2002. View at Publisher · View at Google Scholar · View at PubMed
  53. C. Assisi, M. Stopfer, and M. Bazhenov, “Using the structure of inhibitory networks to unravel mechanisms of spatiotemporal patterning,” Neuron, vol. 69, pp. 373–386, 2011. View at Publisher · View at Google Scholar · View at PubMed
  54. G. Buzsaki and J. J. Chrobak, “Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks,” Current Opinion in Neurobiology, vol. 5, no. 4, pp. 504–510, 1995. View at Publisher · View at Google Scholar