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From Dendrites to Networks: Optically Probing the Living Brain Slice and Using Principal Component Analysis to Characterize Neuronal Morphology

  • Jesse H. Goldberg
  • Farid Hamzei-Sichani
  • Jason MacLean
  • Gabor Tamas
  • Rochelle Urban
  • Rafael Yuste

Abstract

Recently, advances in optical imaging of the living brain slice preparation have permitted neuronal circuitry to be examined at multiple levels, ranging from individual synaptic contacts on dendrites to whole populations of neurons in a network. In this chapter, we describe three techniques that, together, enable a powerful dissection of neuronal circuits across multiple space scales. We describe methods for (1) combining whole-cell recording with two-photon calcium imaging and electron microscopic reconstruction to examine the functions of individual synapses and dendrites during synaptic stimulation, (2) imaging hundreds of neurons in the brain slice simultaneously to examine the spatiotemporal dynamics of activity in living neuronal networks, and (3) performing an unbiased, quantitative analysis of neuronal morphology that is increasingly necessary in light of the multiparametric structural diversity of distinct neuronal subclasses.

Keywords

cluster analysis dendrite imaging microdomain network principal component analysis two-photon calcium 

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References

  1. Alger, B. E., and Teyler, T. J., 1976, Long-term and short-term plasticity in the CA1, CA3, and dentate regions of the rat hippocampal slice, Brain Res. 110:463–480.PubMedCrossRefGoogle Scholar
  2. Allbritton, N. L., Meyer, T., and Stryer, L., 1992, Range of messenger action of calcium ion and inositol 1,4,5-trisphosphate, Science 258:1812–1815.PubMedCrossRefGoogle Scholar
  3. Antic, S., Major, G., Chen, W. R., Wuskel, J., Loew, L., and Zecevic, D., 1997, Fast voltage-sensitive dye recording of membrane potential changes at multiple sites on an individual nerve cell in the rat cortical slice, Biol. Bull. 193:261.PubMedGoogle Scholar
  4. Buhl, E. H., Halasy, K., and Somogyi, P., 1994, Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites, Nature 368:823–828.PubMedCrossRefGoogle Scholar
  5. Cattell, R., 1966, The scree test for the number of factors, Multivariate Behav. Res. 2:245–276.CrossRefGoogle Scholar
  6. Connors, B.W., and Gutnick, M. J., 1990, Intrinsic firing patterns of diverse neocortical neurons, Trends Neurosci. 13:99–104.PubMedCrossRefGoogle Scholar
  7. Cossart, R., Aronov, D., and Yuste, R., 2003, Attractor dynamics of network UP states in neocortex, Nature 423:283–289.PubMedCrossRefGoogle Scholar
  8. Cossart, R., Ikegaya, Y., and Yuste, R., 2005, Calcium imaging of cortical networks dynamics, Cell Calcium 37:451–457.PubMedCrossRefGoogle Scholar
  9. Denk, W., and Svoboda, K., 1997, Photon upmanship: why multiphoton imaging is more than a gimmick, Neuron 18:351–357.PubMedCrossRefGoogle Scholar
  10. Denk, W., Strickler, J. H., and Webb, W. W., 1990, Two-photon laser scanning fluorescence microscopy, Science 248:73–76.PubMedCrossRefGoogle Scholar
  11. Dingledine, R., Dodd, J., and Kelly, J. S., 1980, The in vitro brain slice as a useful neurophysiological preparation for intracellular recording, J. Neurosci. Methods 2:323–362.PubMedCrossRefGoogle Scholar
  12. Euler, T., Detwiler, P. B., and Denk, W., 2002, Directionally selective calcium signals in dendrites of starburst amacrine cells, Nature 418:845–852.PubMedCrossRefGoogle Scholar
  13. Freund, T. F., and Buzsaki, G., 1996, Interneurons of the hippocampus, Hippocampus 6:347–470.PubMedCrossRefGoogle Scholar
  14. Ghozland, S., Aguado, F., Espinosa-Parrilla, J. F., Soriano, E., and Maldonado, R., 2002, Spontaneous network activity of cerebellar granule neurons: impairment by in vivo chronic cannabinoid administration, Eur. J. Neurosci. 16:641–651.PubMedCrossRefGoogle Scholar
  15. Gibson, J. R., Beierlein, M., and Connors, B. W., 1999, Two networks of electrically coupled inhibitory neurons in neocortex, Nature 402:75–79.PubMedCrossRefGoogle Scholar
  16. Goldberg, J., Holthoff, K., and Yuste, R., 2002, A problem with Hebb and local spikes, Trends Neurosci. 25:433.PubMedCrossRefGoogle Scholar
  17. Goldberg, J. H., Tamas, G., Aronov, D., and Yuste, R., 2003c, Calcium microdomains in aspiny dendrites, Neuron 40:807–821.PubMedCrossRefGoogle Scholar
  18. Goldberg, J. H., Tamas, G., and Yuste, R., 2003a, Ca2+ imaging of mouse neocortical interneurone dendrites: Ia-type K+ channels control action potential backpropagation, J. Physiol. 551:49–65.PubMedCrossRefGoogle Scholar
  19. Goldberg, J. H., and Yuste, R., 2005, Space matters: local and global dendritic Ca2+ compartmentalization in cortical interneurons, Trends Neurosci. 28:158–167.PubMedCrossRefGoogle Scholar
  20. Goldberg, J. H., Yuste, R., and Tamas, G., 2003b, Ca2+ imaging of mouse neocortical interneurone dendrites: contribution of Ca2+-permeable AMPA and NMDA receptors to subthreshold Ca2+ dynamics, J. Physiol. 551:67–78.PubMedCrossRefGoogle Scholar
  21. Gupta, A., Wang, Y., and Markram, H., 2000, Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex, Science 287:273–278.PubMedCrossRefGoogle Scholar
  22. Helmchen, F., 1999, Dendrites as biochemical compartments, In: Stuart, G., Spruston, N., and Hausser, M. (eds.), Dendrites, Oxford: Oxford University Press, pp. 161–192.Google Scholar
  23. Helmchen, F., 2002, Raising the speed limit-fast Ca(2+) handling in dendritic spines, Trends Neurosci. 25:438–441 (discussion 441).PubMedCrossRefGoogle Scholar
  24. Holthoff, K., Kovalchuk, Y., Yuste, R., and Konnerth, A., 2004, Single-shock LTD by local dendritic spikes in pyramidal neurons of mouse visual cortex, J. Physiol. 560:27–36.PubMedCrossRefGoogle Scholar
  25. Horikawa, K., and Armstrong, W. E., 1988, A versatile means of intracellular labeling: injection of biocytin and its detection with avidin conjugates, J. Neurosci. Methods 25:1–11.PubMedCrossRefGoogle Scholar
  26. Ikegaya, Y., Aaron, G., Cossart, R., Aronov, D., Lampl, I., Ferster, D., and Yuste, R., 2004, Synfire chains and cortical songs: temporal modules of cortical activity, Science 304:559–564.PubMedCrossRefGoogle Scholar
  27. Jolliffe, I. T., 1972, Discarding variables in a principal component analyis. I: artificial data, Appl. Stat. 21:160–173.CrossRefGoogle Scholar
  28. Jolliffe, I. T., 2002, Principal component analysis, Springer Series in Statistics, 2nd ed., New York: Springer-Verlag.Google Scholar
  29. Kaiser, H. F., 1960, The application of electronic computers to factor analysis, Educ. Psychol. Meas. 20:141–151.Google Scholar
  30. Majewska, A., Yiu, G., and Yuste, R., 2000, A custom-made two-photon microscope and deconvolution system, Pflügers Arch.—Eur. J. Physiol. 441:398–409.CrossRefGoogle Scholar
  31. Mao, B. Q., Hamzei-Sichani, F., Aronov, D., Froemke, R. C., and Yuste, R., 2001, Dynamics of spontaneous activity in neocortical slices, Neuron 32:883–898.PubMedCrossRefGoogle Scholar
  32. Mao, L., and Wang, J. Q., 2003, Group I metabotropic glutamate receptor-mediated calcium signaling and immediate early gene expression in cultured rat striatal neurons, Eur. J. Neurosci. 17:741–750.PubMedCrossRefGoogle Scholar
  33. Markram, H., Luebke, J., Frotscher, M., and Sakmann, B., 1997, Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs, Science 275:213–215.PubMedCrossRefGoogle Scholar
  34. Markram, H., Toledo-Rodriguez, M., Wang, Y., Gupta, A., Silberberg, G., and Wu, C., 2004, Interneurons of the neocortical inhibitory system, Nat. Rev. Neurosci. 5:793–807.PubMedCrossRefGoogle Scholar
  35. McBain, C. J., and Fisahn, A., 2001, Interneurons unbound, Nat. Rev. Neurosci. 2:11–23.PubMedCrossRefGoogle Scholar
  36. Neher, E., 1998, Usefulness and limitations of linear approximations to the understanding of Ca++ signals, Cell Calcium 24:345–375.PubMedCrossRefGoogle Scholar
  37. Nikolenko, V., Nemet, B., and Yuste, R., 2003, A two-photon and second-harmonic microscope, Methods 30:3–15.PubMedCrossRefGoogle Scholar
  38. Ohki, K., Chung, S., Ch’ng, Y. H., Kara, P., and Reid, R. C., 2005, Functional imaging with cellular resolution reveals precise microarchitecture in visual cortex, Nature 433: 597–603.PubMedCrossRefGoogle Scholar
  39. Petersen, C. C., and Sakmann, B., 2001, Functionally independent columns of rat somatosensory barrel cortex revealed with voltage-sensitive dye imaging, J. Neurosci. 21:8435–8446.PubMedGoogle Scholar
  40. Poirazi, P., and Mel, B. W., 2001, Impact of active dendrites and structural plasticity on the memory capacity of neural tissue, Neuron 29:779–796.PubMedCrossRefGoogle Scholar
  41. Prince, D. A., and Connors, B. W., 1984, Mechanisms of epileptogenesis in cortical structures, Ann. Neurol. 16:S59–S64.PubMedCrossRefGoogle Scholar
  42. Rose, C. R., and Konnerth, A., 2001, NMDA receptor-mediated Na+ signals in spines and dendrites, J. Neurosci. 21:4207–4214.PubMedGoogle Scholar
  43. Rose, C., Kovalchuk, Y., Eilers, J., and Konnerth, A., 1999, Two-photon Na+ imaging in spines and fine dendrites of central neurons, Pflugers Arch. 439:201–207.PubMedCrossRefGoogle Scholar
  44. Sabatini, B. L., Oertner, T. G., and Svoboda, K., 2002, The life cycle of Ca(2+) ions in dendritic spines. Neuron 33:439–452.PubMedCrossRefGoogle Scholar
  45. Sakmann, B., and Neher, E., 1983, Single Channel Recording, New York: Plenum Press.Google Scholar
  46. Sarvey, J. M., Burgard, E. C., and Decker, G., 1989, Long-term potentiation: studies in the hippocampal slice, J. Neurosci. Methods 28:109–124.PubMedCrossRefGoogle Scholar
  47. Schiller, J., Major, G., Koester, H. J., and Schiller, Y., 2000, NMDA spikes in basal dendrites of cortical pyramidal neurons, Nature 404:285–289.PubMedCrossRefGoogle Scholar
  48. Smetters, D. K., Majewska, A., and Yuste, R., 1999, Detecting action potentials in neuronal populations with calcium imaging, Methods 18:215–221.PubMedCrossRefGoogle Scholar
  49. Somogyi, P., Tamas, G., Lujan, R., and Buhl, E., 1998, Salient features of synaptic organisation in the cerebral cortex, Brain Res. Brain Res. Rev. 26:113–135.PubMedCrossRefGoogle Scholar
  50. Spruston, N., Schiller, Y., Stuart, G., and Sakmann, B., 1995, Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites, Science 286:297–300.CrossRefGoogle Scholar
  51. Stosiek, C., Garaschuk, O., Holthoff, K., and Konnerth, A., 2003, In vivo two-photon calcium imaging of neuronal networks, Proc. Natl. Acad. Sci. U. S. A. 100:7319–7324.PubMedCrossRefGoogle Scholar
  52. Tamas, G., Buhl, E. H., Lorincz, A., and Somogyi, P., 2000, Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons, Nat. Neurosci. 3:366–371.PubMedCrossRefGoogle Scholar
  53. Tamas, G., Buhl, E. H., and Somogyi, P., 1997, Massive autaptic self-innervation of GABAergic neurons in cat visual cortex, J. Neurosci. 17:6352–6364.PubMedGoogle Scholar
  54. Tanaka, E., Uchikado, H., Niiyama, S., Uematsu, K., and Higashi, H., 2002, Extrusion of intracellular calcium ion after in vitro ischemia in the rat hippocampal CA1 region, J. Neurophysiol. 88:879–887.PubMedGoogle Scholar
  55. Tsien, R. Y., 1981, A nondisruptive technique for loading calcium buffers and indicators into cells, Nature 290:527–528.PubMedCrossRefGoogle Scholar
  56. Tsien, R. Y., 1989, Fluorescent probes of cell signaling, Ann. Rev. Neurosci. 12:227–253.PubMedCrossRefGoogle Scholar
  57. Voitenko, N. V., Kostyuk, E. P., Kruglikov, I. A., and Kostyuk, P. G., 1999, Changes in calcium signaling in dorsal horn neurons in rats with streptozotocin-induced diabetes, Neuroscience 94:887–890.PubMedCrossRefGoogle Scholar
  58. Waters, J., Schaefer, A., and Sakmann, B., 2005, Backpropagating action potentials in neurones: measurement, mechanisms, and potential functions, Prog. Biophys. Mol. Biol. 87:145–170.PubMedCrossRefGoogle Scholar
  59. Yuste, R., and Denk, W., 1995, Dendritic spines as basic units of synaptic integration, Nature 375:682–684.PubMedCrossRefGoogle Scholar
  60. Yuste, R., Gutnick, M. J., Saar, D., Delaney, K. D., and Tank, D. W., 1994, Calcium accumulations in dendrites from neocortical neurons: an apical band and evidence for functional compartments, Neuron 13:23–43.PubMedCrossRefGoogle Scholar
  61. Yuste, R., and Katz, L. C., 1991, Control of postsynaptic Ca2+ influx in developing neocortex by excitatory and inhibitory neurotransmitters, Neuron 6:333–344.PubMedCrossRefGoogle Scholar
  62. Yuste, R., Tank, D.W., and Kleinfeld, D., 1997, Functional study of the rat cortical microcircuitry with voltage-sensitive dye imaging of neocortical slices, Cereb. Cortex 6/7:546–558.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Jesse H. Goldberg
    • 1
  • Farid Hamzei-Sichani
    • 4
  • Jason MacLean
    • 2
  • Gabor Tamas
    • 5
  • Rochelle Urban
    • 2
  • Rafael Yuste
    • 3
  1. 1.McGovern Institute for Brain and Cognitive SciencesMassachusetts Institute of TechnologyCambridge
  2. 2.Department of Biological SciencesColumbia UniversityNew York
  3. 3.Howard Hughes Medical Institute, Department of Biological SciencesColumbia UniversityNew York
  4. 4.Department of Physiology and PharmacologyState University of New York, Downstate Medical CenterBrooklyn
  5. 5.Department of Comparative PhysiologyUniversity of SzegedSzegedHungary

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