Table of Contents Author Guidelines Submit a Manuscript
Neural Plasticity
Volume 2015 (2015), Article ID 573543, 13 pages
http://dx.doi.org/10.1155/2015/573543
Research Article

Diverse Short-Term Dynamics of Inhibitory Synapses Converging on Striatal Projection Neurons: Differential Changes in a Rodent Model of Parkinson’s Disease

1División de Neurociencias, Instituto de Fisiología Celular, Universidad Nacional Autónoma de México, 04510 Ciudad de México, Mexico
2Departamento de Matemáticas, Facultad de Ciencias, Universidad Nacional Autónoma de México, 04510 Ciudad de México, Mexico

Received 19 March 2015; Accepted 20 May 2015

Academic Editor: Marco Atzori

Copyright © 2015 Janet Barroso-Flores et al. 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. L. F. Abbott and W. G. Regehr, “Synaptic computation,” Nature, vol. 431, no. 7010, pp. 796–803, 2004. View at Publisher · View at Google Scholar · View at Scopus
  2. G. Silberberg, S. Grillner, F. E. N. LeBeau, R. Maex, and H. Markram, “Synaptic pathways in neural microcircuits,” Trends in Neurosciences, vol. 28, no. 10, pp. 541–551, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. M. H. Hennig, “Theoretical models of synaptic short term plasticity,” Frontiers in Computational Neuroscience, vol. 7, article 45, 2013. View at Publisher · View at Google Scholar · View at Scopus
  4. J. S. Dittman, A. C. Kreitzer, and W. G. Regehr, “Interplay between facilitation, depression, and residual calcium at three presynaptic terminals,” Journal of Neuroscience, vol. 20, no. 4, pp. 1374–1385, 2000. View at Google Scholar · View at Scopus
  5. A. M. Thomson, “Facilitation, augmentation and potentiation at central synapses,” Trends in Neurosciences, vol. 23, no. 7, pp. 305–312, 2000. View at Publisher · View at Google Scholar · View at Scopus
  6. R. S. Zucker and W. G. Regehr, “Short-term synaptic plasticity,” Annual Review of Physiology, vol. 64, no. 1, pp. 355–405, 2002. View at Publisher · View at Google Scholar · View at Scopus
  7. W. A. Catterall and A. P. Few, “Calcium channel regulation and presynaptic plasticity,” Neuron, vol. 59, no. 6, pp. 882–901, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. S. Mochida, A. P. Few, T. Scheuer, and W. A. Catterall, “Regulation of presynaptic CaV2.1 channels by Ca2+ sensor proteins mediates short-term synaptic Plasticity,” Neuron, vol. 57, no. 2, pp. 210–216, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. D. Fioravante and W. G. Regehr, “Short-term forms of presynaptic plasticity,” Current Opinion in Neurobiology, vol. 21, no. 2, pp. 269–274, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. R. Dutta Roy, M. I. Stefan, and C. Rosenmund, “Biophysical properties of presynaptic short-term plasticity in hippocampal neurons: insights from electrophysiology, imaging and mechanistic models,” Frontiers in Cellular Neuroscience, vol. 8, article 141, 2014. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Beierlein, J. R. Gibson, and B. W. Connors, “Two dynamically distinct inhibitory networks in layer 4 of the neocortex,” Journal of Neurophysiology, vol. 90, no. 5, pp. 2987–3000, 2003. View at Publisher · View at Google Scholar · View at Scopus
  12. G. Silberberg, C. Wu, and H. Markram, “Synaptic dynamics control the timing of neuronal excitation in the activated neocortical microcircuit,” The Journal of Physiology, vol. 556, no. 1, pp. 19–27, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. T. Branco and K. Staras, “The probability of neurotransmitter release: variability and feedback control at single synapses,” Nature Reviews Neuroscience, vol. 10, no. 5, pp. 373–383, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. A. V. Blackman, T. Abrahamsson, R. P. Costa, T. Lalanne, and P. J. Sjöström, “Target-cell-specific short-term plasticity in local circuits,” Frontiers in Synaptic Neuroscience, vol. 5, article 11, 2013. View at Publisher · View at Google Scholar
  15. Y. Ma, H. Hu, and A. Agmon, “Short-term plasticity of unitary inhibitory-to-inhibitory synapses depends on the presynaptic interneuron subtype,” The Journal of Neuroscience, vol. 32, no. 3, pp. 983–988, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. S. Savanthrapadian, T. Meyer, C. Elgueta, S. A. Booker, I. Vida, and M. Bartos, “Synaptic properties of SOM- and CCK-expressing cells in dentate gyrus interneuron networks,” The Journal of Neuroscience, vol. 34, no. 24, pp. 8197–8209, 2014. View at Publisher · View at Google Scholar
  17. A. Reyes, R. Lujan, A. Rozov, N. Burnashev, P. Somogyi, and B. Sakmann, “Target-cell-specific facilitation and depression in neocortical circuits,” Nature Neuroscience, vol. 1, no. 4, pp. 279–285, 1998. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Gupta, Y. Wang, and H. Markram, “Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex,” Science, vol. 287, no. 5451, pp. 273–278, 2000. View at Publisher · View at Google Scholar · View at Scopus
  19. Y. Wang, H. Markram, P. H. Goodman, T. K. Berger, J. Ma, and P. S. Goldman-Rakic, “Heterogeneity in the pyramidal network of the medial prefrontal cortex,” Nature Neuroscience, vol. 9, no. 4, pp. 534–542, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. F. Tecuapetla, L. Carrillo-Reid, J. Bargas, and E. Galarraga, “Dopaminergic modulation of short-term synaptic plasticity at striatal inhibitory synapses,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 24, pp. 10258–10263, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. O. Ibáñez-Sandoval, F. Tecuapetla, B. Unal, F. Shah, T. Koós, and J. M. Tepper, “A novel functionally distinct subtype of striatal neuropeptide Y interneuron,” The Journal of Neuroscience, vol. 31, no. 46, pp. 16757–16769, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. A. H. Gittis and A. C. Kreitzer, “Striatal microcircuitry and movement disorders,” Trends in Neurosciences, vol. 35, no. 9, pp. 557–564, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. S. L. Jackman, B. M. Beneduce, I. R. Drew, and W. G. Regehr, “Achieving high-frequency optical control of synaptic transmission,” The Journal of Neuroscience, vol. 34, no. 22, pp. 7704–7714, 2014. View at Publisher · View at Google Scholar · View at Scopus
  24. W. A. Catterall, K. Leal, and E. Nanou, “Calcium channels and short-term synaptic plasticity,” The Journal of Biological Chemistry, vol. 288, no. 15, pp. 10742–10749, 2013. View at Publisher · View at Google Scholar · View at Scopus
  25. T. Koos, J. M. Tepper, and C. J. Wilson, “Comparison of IPSCs evoked by spiny and fast-spiking neurons in the neostriatum,” The Journal of Neuroscience, vol. 24, no. 36, pp. 7916–7922, 2004. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Taverna, E. Ilijic, and D. J. Surmeier, “Recurrent collateral connections of striatal medium spiny neurons are disrupted in models of Parkinson's disease,” Journal of Neuroscience, vol. 28, no. 21, pp. 5504–5512, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. N. Dehorter, C. Guigoni, C. Lopez et al., “Dopamine-deprived striatal GABAergic interneurons burst and generate repetitive gigantic IPSCs in medium spiny neurons,” Journal of Neuroscience, vol. 29, no. 24, pp. 7776–7787, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. V. G. López-Huerta, L. Carrillo-Reid, E. Galarraga et al., “The balance of striatal feedback transmission is disrupted in a model of parkinsonism,” The Journal of Neuroscience, vol. 33, no. 11, pp. 4964–4975, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. R. K. W. Schwarting and J. P. Huston, “The unilateral 6-hydroxydopamine lesion model in behavioral brain research. Analysis of functional deficits, recovery and treatments,” Progress in Neurobiology, vol. 50, no. 2-3, pp. 275–331, 1996. View at Publisher · View at Google Scholar · View at Scopus
  30. E. Flores-Barrera, B. J. Vizcarra-Chacón, D. Tapia, J. Bargas, and E. Galarraga, “Different corticostriatal integration in spiny projection neurons from direct and indirect pathways,” Frontiers in Systems Neuroscience, vol. 4, article 15, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. V. G. López-Huerta, E. Blanco-Hernández, J. Bargas, and E. Galarraga, “Presynaptic modulation by somatostatin in the rat neostriatum is altered in a model of parkinsonism,” Journal of Neurophysiology, vol. 108, no. 4, pp. 1032–1043, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. E. Galarraga, C. Vilchis, T. Tkatch et al., “Somatostatinergic modulation of firing pattern and calcium-activated potassium currents in medium spiny neostriatal neurons,” Neuroscience, vol. 146, no. 2, pp. 537–554, 2007. View at Publisher · View at Google Scholar · View at Scopus
  33. R. Hernández-Martínez, J. J. Aceves, P. E. Rueda-Orozco et al., “Muscarinic presynaptic modulation in GABAergic pallidal synapses of the rat,” Journal of Neurophysiology, vol. 113, no. 3, pp. 796–807, 2015. View at Publisher · View at Google Scholar
  34. F. Tecuapetla, L. Carrillo-Reid, J. N. Guzmán, E. Galarraga, and J. Bargas, “Different inhibitory inputs onto neostriatal projection neurons as revealed by field stimulation,” Journal of Neurophysiology, vol. 93, no. 2, pp. 1119–1126, 2005. View at Publisher · View at Google Scholar · View at Scopus
  35. A. B. Muñoz-Manchado, C. Foldi, S. Szydlowski et al., “Novel striatal gabaergic interneuron populations labeled in the 5HT3aEGFP mouse,” Cerebral Cortex, 2014. View at Publisher · View at Google Scholar
  36. U. Czubayko and D. Plenz, “Fast synaptic transmission between striatal spiny projection neurons,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 24, pp. 15764–15769, 2002. View at Publisher · View at Google Scholar · View at Scopus
  37. J. N. Guzmán, A. Hernández, E. Galarraga et al., “Dopaminergic modulation of axon collaterals interconnecting spiny neurons of the rat striatum,” The Journal of Neuroscience, vol. 23, no. 26, pp. 8931–8940, 2003. View at Google Scholar · View at Scopus
  38. J. M. Tepper and J. P. Bolam, “Functional diversity and specificity of neostriatal interneurons,” Current Opinion in Neurobiology, vol. 14, no. 6, pp. 685–692, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. J. M. Tepper, T. Koós, and C. J. Wilson, “GABAergic microcircuits in the neostriatum,” Trends in Neurosciences, vol. 27, no. 11, pp. 662–669, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. J. M. Tepper, C. J. Wilson, and T. Koós, “Feedforward and feedback inhibition in neostriatal GABAergic spiny neurons,” Brain Research Reviews, vol. 58, no. 2, pp. 272–281, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. J. M. Tepper, F. Tecuapetla, T. Koós, and O. Ibáñez-Sandoval, “Heterogeneity and diversity of striatal GABAergic interneurons,” Frontiers in Neuroanatomy, vol. 4, article 150, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. O. Ibáñez-Sandoval, F. Tecuapetla, B. Unal, F. Shah, T. Koós, and J. M. Tepper, “Electrophysiological and morphological characteristics and synaptic connectivity of tyrosine hydroxylase-expressing neurons in adult mouse striatum,” Journal of Neuroscience, vol. 30, no. 20, pp. 6999–7016, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. J. A. Beatty, S. C. Song, and C. J. Wilson, “Cell-type-specific resonances shape the responses of striatal neurons to synaptic input,” Journal of Neurophysiology, vol. 113, no. 3, pp. 688–700, 2015. View at Publisher · View at Google Scholar
  44. G. Russo, T. R. Nieus, S. Maggi, and S. Taverna, “Dynamics of action potential firing in electrically connected striatal fast-spiking interneurons,” Frontiers in Cellular Neuroscience, vol. 7, article 209, 2013. View at Publisher · View at Google Scholar · View at Scopus
  45. S. N. Szydlowski, I. Pollak Dorocic, H. Planert, M. Carlén, K. Meletis, and G. Silberberg, “Target selectivity of feedforward inhibition by striatal fast-spiking interneurons,” The Journal of Neuroscience, vol. 33, no. 4, pp. 1678–1683, 2013. View at Publisher · View at Google Scholar · View at Scopus
  46. O. Jáidar, L. Carrillo-Reid, A. Hernández, R. Drucker-Colín, J. Bargas, and A. Hernández-Cruz, “Dynamics of the Parkinsonian striatal microcircuit: entrainment into a dominant network state,” The Journal of Neuroscience, vol. 30, no. 34, pp. 11326–11336, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. J. D. Clements and R. A. Silve, “Unveiling synaptic plasticity: a new graphical and analytical approach,” Trends in Neurosciences, vol. 23, no. 3, pp. 105–113, 2000. View at Publisher · View at Google Scholar · View at Scopus